Skip to main content
Top
Published in: BMC Complementary Medicine and Therapies 1/2013

Open Access 01-12-2013 | Research article

The hexane fraction of Ardisia crispa Thunb. A. DC. roots inhibits inflammation-induced angiogenesis

Authors: Dayang Erna Zulaikha Awang Hamsin, Roslida Abdul Hamid, Latifah Saiful Yazan, Che Norma Mat Taib, Yeong Looi Ting

Published in: BMC Complementary Medicine and Therapies | Issue 1/2013

Login to get access

Abstract

Background

Ardisia crispa (Myrsinaceae) is used in traditional Malay medicine to treat various ailments associated with inflammation, including rheumatism. The plant’s hexane fraction was previously shown to inhibit several diseases associated with inflammation. As there is a strong correlation between inflammation and angiogenesis, we conducted the present study to investigate the anti-angiogenic effects of the plant’s roots in animal models of inflammation-induced angiogenesis.

Methods

We first performed phytochemical screening and high-performance liquid chromatography (HPLC) fingerprinting of the hexane fraction of Ardisia crispa roots ethanolic extract (ACRH) and its quinone-rich fraction (QRF). The anti-inflammatory properties of ACRH and QRF were tested using the Miles vascular permeability assay and the murine air pouch granuloma model following oral administration at various doses.

Results

Preliminary phytochemical screening of ACRH revealed the presence of flavonoids, triterpenes, and tannins. The QRF was separated from ACRH (38.38% w/w) by column chromatography, and was isolated to yield a benzoquinonoid compound. The ACRH and QRF were quantified by HPLC. The LD50 value of ACRH was 617.02 mg/kg. In the Miles vascular permeability assay, the lowest dose of ACRH (10 mg/kg) and all doses of QRF significantly reduced vascular endothelial growth factor (VEGF)-induced hyperpermeability, when compared with the vehicle control. In the murine air pouch granuloma model, ACRH and QRF both displayed significant and dose-dependent anti-inflammatory effects, without granuloma weight. ACRH and QRF significantly reduced the vascular index, but not granuloma tissue weight.

Conclusions

In conclusion, both ACRH and QRF showed potential anti-inflammatory properties in a model of inflammation-induced angiogenesis model, demonstrating their potential anti-angiogenic properties.
Appendix
Available only for authorised users
Literature
1.
go back to reference Woo AYH, Zhao Y, Zhang R, Zhou Z, Cheng CHK: Angiogenesis and Chinese medicinal foods. Anti-angiogenic functional and medicinal foods. Edited by: Losso JN, Shahidi F, Bagchi D. 2007, New York: CRC Press, 581-592.CrossRef Woo AYH, Zhao Y, Zhang R, Zhou Z, Cheng CHK: Angiogenesis and Chinese medicinal foods. Anti-angiogenic functional and medicinal foods. Edited by: Losso JN, Shahidi F, Bagchi D. 2007, New York: CRC Press, 581-592.CrossRef
2.
go back to reference Folkman J: Tumor angiogenesis: therapeutic implications. New Engl J Med. 1971, 285 (21): 1182-1186. 10.1056/NEJM197111182852108.CrossRefPubMed Folkman J: Tumor angiogenesis: therapeutic implications. New Engl J Med. 1971, 285 (21): 1182-1186. 10.1056/NEJM197111182852108.CrossRefPubMed
3.
go back to reference Folkman J: Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med. 1995, 1 (1): 27-31. 10.1038/nm0195-27.CrossRefPubMed Folkman J: Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med. 1995, 1 (1): 27-31. 10.1038/nm0195-27.CrossRefPubMed
4.
go back to reference Khurana R, Simmons M, Martin JF, Zachary IC: Role of angiogenesis in cardiovascular disease: a critical appraisal. Circulation. 2005, 112 (12): 1813-1824. 10.1161/CIRCULATIONAHA.105.535294.CrossRefPubMed Khurana R, Simmons M, Martin JF, Zachary IC: Role of angiogenesis in cardiovascular disease: a critical appraisal. Circulation. 2005, 112 (12): 1813-1824. 10.1161/CIRCULATIONAHA.105.535294.CrossRefPubMed
5.
go back to reference Nakano T, Nakashima Y, Yonemitsu Y, Sumiyoshi S, Chen YX, Akishima Y, Iida M, Sueishi K: Angiogenesis and lymphangiogenesis and the expression of lymphangiogenic factors in the atherosclerotic intima of human coronary arteries. Hum Pathol. 2005, 36 (4): 330-340. 10.1016/j.humpath.2005.01.001.CrossRefPubMed Nakano T, Nakashima Y, Yonemitsu Y, Sumiyoshi S, Chen YX, Akishima Y, Iida M, Sueishi K: Angiogenesis and lymphangiogenesis and the expression of lymphangiogenic factors in the atherosclerotic intima of human coronary arteries. Hum Pathol. 2005, 36 (4): 330-340. 10.1016/j.humpath.2005.01.001.CrossRefPubMed
6.
go back to reference Chen F, Eriksson P, Kimura T, Herzfeld I, Valen G: Apoptosis and angiogenesis are induced in the unstable atherosclerotic plaque. Coron Artery Dis. 2005, 16 (3): 191-197. 10.1097/00019501-200505000-00009.CrossRefPubMed Chen F, Eriksson P, Kimura T, Herzfeld I, Valen G: Apoptosis and angiogenesis are induced in the unstable atherosclerotic plaque. Coron Artery Dis. 2005, 16 (3): 191-197. 10.1097/00019501-200505000-00009.CrossRefPubMed
7.
go back to reference Hayden MR, Tyagi SC: Vasa vasorum in plaque angiogenesis, metabolic syndrome, type 2 diabetes mellitus, and atheroscleropathy: a malignant transformation. Cardiovasc Diabetol. 2004, 3: 1-6. 10.1186/1475-2840-3-1.CrossRefPubMedPubMedCentral Hayden MR, Tyagi SC: Vasa vasorum in plaque angiogenesis, metabolic syndrome, type 2 diabetes mellitus, and atheroscleropathy: a malignant transformation. Cardiovasc Diabetol. 2004, 3: 1-6. 10.1186/1475-2840-3-1.CrossRefPubMedPubMedCentral
8.
go back to reference Walsh DA, Pearson CI: Angiogenesis in the pathogenesis of inflammatory joint and lung diseases. Arthritis Res Ther. 2001, 3 (3): 147-153. 10.1186/ar292.CrossRef Walsh DA, Pearson CI: Angiogenesis in the pathogenesis of inflammatory joint and lung diseases. Arthritis Res Ther. 2001, 3 (3): 147-153. 10.1186/ar292.CrossRef
9.
go back to reference Weipeng B, Fei C, Ling B, Ping Z, Wenxin Q: Dihydrotanshinone I inhibits angiogenesis both in vitro and in vivo. Acta Biochim Biophys Sin. 2008, 40: 1-6. 10.1111/j.1745-7270.2008.00370.x.CrossRef Weipeng B, Fei C, Ling B, Ping Z, Wenxin Q: Dihydrotanshinone I inhibits angiogenesis both in vitro and in vivo. Acta Biochim Biophys Sin. 2008, 40: 1-6. 10.1111/j.1745-7270.2008.00370.x.CrossRef
10.
go back to reference Shishodia S, Sethi G, Aggrawal BB: Curcumin: getting back to the roots. Ann N Y Acad Sci. 2005, 1056 (1): 206-217. 10.1196/annals.1352.010.CrossRefPubMed Shishodia S, Sethi G, Aggrawal BB: Curcumin: getting back to the roots. Ann N Y Acad Sci. 2005, 1056 (1): 206-217. 10.1196/annals.1352.010.CrossRefPubMed
11.
go back to reference Raso GM, Meli R, Di Carlo G, Pacilio M, Di Carlo R: Inhibition of inducible NO synthase and cyclooxygenase-2 expression by flavonoids in macrophage J774A. Life Sci. 2001, 68 (8): 921-931. 10.1016/S0024-3205(00)00999-1.CrossRefPubMed Raso GM, Meli R, Di Carlo G, Pacilio M, Di Carlo R: Inhibition of inducible NO synthase and cyclooxygenase-2 expression by flavonoids in macrophage J774A. Life Sci. 2001, 68 (8): 921-931. 10.1016/S0024-3205(00)00999-1.CrossRefPubMed
12.
go back to reference Shimamura M, Hazato T, Ashino H, Yamamoto Y, Iwasaki E, Tobe H, Yamamoto K, Yamamoto S: Inhibition of angiogenesis by humulone; a bitter acid from beer hop. Biochem Biophys Res Commun. 2001, 289 (1): 220-224. 10.1006/bbrc.2001.5934.CrossRefPubMed Shimamura M, Hazato T, Ashino H, Yamamoto Y, Iwasaki E, Tobe H, Yamamoto K, Yamamoto S: Inhibition of angiogenesis by humulone; a bitter acid from beer hop. Biochem Biophys Res Commun. 2001, 289 (1): 220-224. 10.1006/bbrc.2001.5934.CrossRefPubMed
13.
go back to reference Kwon HJ, Shim JS, Kim JH, Cho HY, Yum YN, Kim SH, Yu J: Betulinic acid inhibits growth factor-induced angiogenesis via the modulation of mitochondrial function in endothelial cells. Jpn J Cancer Res. 2002, 93 (4): 417-425. 10.1111/j.1349-7006.2002.tb01273.x.CrossRefPubMed Kwon HJ, Shim JS, Kim JH, Cho HY, Yum YN, Kim SH, Yu J: Betulinic acid inhibits growth factor-induced angiogenesis via the modulation of mitochondrial function in endothelial cells. Jpn J Cancer Res. 2002, 93 (4): 417-425. 10.1111/j.1349-7006.2002.tb01273.x.CrossRefPubMed
14.
go back to reference Surh YJ: Anti-tumor promoting potential of selected spice ingredients with antioxidative and anti-inflammatory activities: a short review. Food Chem Toxicol. 2002, 40 (8): 1091-1097. 10.1016/S0278-6915(02)00037-6.CrossRefPubMed Surh YJ: Anti-tumor promoting potential of selected spice ingredients with antioxidative and anti-inflammatory activities: a short review. Food Chem Toxicol. 2002, 40 (8): 1091-1097. 10.1016/S0278-6915(02)00037-6.CrossRefPubMed
15.
go back to reference Bråkenhielm E, Cao R, Cao Y: Suppression of angiogenesis, tumor growth, and wound healing by resveratrol, a natural compound in red wine and grapes. FASEB J. 2001, 15 (10): 1798-1800.PubMed Bråkenhielm E, Cao R, Cao Y: Suppression of angiogenesis, tumor growth, and wound healing by resveratrol, a natural compound in red wine and grapes. FASEB J. 2001, 15 (10): 1798-1800.PubMed
16.
go back to reference Delmas D, Lançon A, Colin D, Jannin B, Latruffe N: Resveratrol as a chemopreventive agent: a promising molecule for fighting cancer. Curr Drug Targets. 2006, 7 (4): 423-442. 10.2174/138945006776359331.CrossRefPubMed Delmas D, Lançon A, Colin D, Jannin B, Latruffe N: Resveratrol as a chemopreventive agent: a promising molecule for fighting cancer. Curr Drug Targets. 2006, 7 (4): 423-442. 10.2174/138945006776359331.CrossRefPubMed
17.
go back to reference Foitzik T, Hotz HG, Hotz B, Wittig F, Buhr HJ: Selective inhibition of cyclooxygenase-2 (COX-2) reduces prostaglandin E2 production and attenuates systemic disease sequelae in experimental pancreatitis. Hepatogastroenterology. 2003, 50 (52): 1159-1162.PubMed Foitzik T, Hotz HG, Hotz B, Wittig F, Buhr HJ: Selective inhibition of cyclooxygenase-2 (COX-2) reduces prostaglandin E2 production and attenuates systemic disease sequelae in experimental pancreatitis. Hepatogastroenterology. 2003, 50 (52): 1159-1162.PubMed
18.
go back to reference Hoper MM, Voelkel NF, Bates TQ, Allard JD, Horan M, Shepherd D, Tudier R: Prostaglandin induce VEGF growth factor in human monocytic cell lines and rat lungs via cAMP. Am J Respir Cell Mol Biol. 1997, 17 (6): 748-756.CrossRefPubMed Hoper MM, Voelkel NF, Bates TQ, Allard JD, Horan M, Shepherd D, Tudier R: Prostaglandin induce VEGF growth factor in human monocytic cell lines and rat lungs via cAMP. Am J Respir Cell Mol Biol. 1997, 17 (6): 748-756.CrossRefPubMed
19.
go back to reference Romano M, Claria J: Cyclooxygenase-2 and 5-lipoxygenase converging function on cell proliferation and angiogenesis: implication for cancer therapy. FASEB J. 2003, 17 (14): 1986-1995. 10.1096/fj.03-0053rev.CrossRefPubMed Romano M, Claria J: Cyclooxygenase-2 and 5-lipoxygenase converging function on cell proliferation and angiogenesis: implication for cancer therapy. FASEB J. 2003, 17 (14): 1986-1995. 10.1096/fj.03-0053rev.CrossRefPubMed
20.
go back to reference Heyne K: Tumbuhan berguna Indonesia III, translated by Badan Litbang Kehutanan Jakarta. 1987, Indonesia: Yayasan Sarana Wana Jaya Heyne K: Tumbuhan berguna Indonesia III, translated by Badan Litbang Kehutanan Jakarta. 1987, Indonesia: Yayasan Sarana Wana Jaya
21.
go back to reference Muhammad Z, Mustafa AM: Traditional Malay Medicinal Plants. 1994, Kuala Lumpur: Fajar Bakti, 39-41. Muhammad Z, Mustafa AM: Traditional Malay Medicinal Plants. 1994, Kuala Lumpur: Fajar Bakti, 39-41.
22.
go back to reference Jansakul C, Herbert B, Lennart K, Gunnar S: Ardisiacrispin A and B, two utero-contacting saponins from Ardisia crispa. Planta Medica. 1987, 53 (5): 405-409. 10.1055/s-2006-962758.CrossRefPubMed Jansakul C, Herbert B, Lennart K, Gunnar S: Ardisiacrispin A and B, two utero-contacting saponins from Ardisia crispa. Planta Medica. 1987, 53 (5): 405-409. 10.1055/s-2006-962758.CrossRefPubMed
23.
go back to reference Yoshida K, Koma Y, Kikuchi H: Therapeutic substance FR-900359 from Ardisia crispa. Japan Kokkai Tokyo Kobo JP. 1987, 283: 917-920. Yoshida K, Koma Y, Kikuchi H: Therapeutic substance FR-900359 from Ardisia crispa. Japan Kokkai Tokyo Kobo JP. 1987, 283: 917-920.
24.
go back to reference Kang YH, Kim WH, Park MK, Han BH: Antimetastatic and antitumor effects of benzoquuinonoid AC7-1 from Ardisia crispa. Int J Cancer. 2001, 93 (5): 736-740. 10.1002/ijc.1384.CrossRefPubMed Kang YH, Kim WH, Park MK, Han BH: Antimetastatic and antitumor effects of benzoquuinonoid AC7-1 from Ardisia crispa. Int J Cancer. 2001, 93 (5): 736-740. 10.1002/ijc.1384.CrossRefPubMed
25.
go back to reference Roslida AH, Teh YH, Kim KH: Evaluation of anti-ulcer activity of Ardisia crispa Thunb. D.C. PharmacognRes. 2009, 1: 250-255. Roslida AH, Teh YH, Kim KH: Evaluation of anti-ulcer activity of Ardisia crispa Thunb. D.C. PharmacognRes. 2009, 1: 250-255.
26.
go back to reference Roslida AH, Kim KH: Anti-inflammatory effect and anti-hyperalgesic effect of Ardisia crispa Thunb D C. Pharmacogn Mag. 2008, 4: 262-268. Roslida AH, Kim KH: Anti-inflammatory effect and anti-hyperalgesic effect of Ardisia crispa Thunb D C. Pharmacogn Mag. 2008, 4: 262-268.
27.
go back to reference Roslida AH: Anti-inflammatory and analgesic effects of AC-2 isolated from Ardisia crispa are mediated via COX-2 inhibition. 2004, Kuala Lumpur, Malaysia: PhD thesis, Universiti Malaya, Physiology Department Roslida AH: Anti-inflammatory and analgesic effects of AC-2 isolated from Ardisia crispa are mediated via COX-2 inhibition. 2004, Kuala Lumpur, Malaysia: PhD thesis, Universiti Malaya, Physiology Department
28.
go back to reference Jackson JR, Seed MP, Kircher CH, Willoughby DA, Winkler JD: The codependence of angiogenesis and chronic inflammation. FASEB J. 1997, 11 (6): 457-465.PubMed Jackson JR, Seed MP, Kircher CH, Willoughby DA, Winkler JD: The codependence of angiogenesis and chronic inflammation. FASEB J. 1997, 11 (6): 457-465.PubMed
29.
go back to reference Wang W, Bergh A, Damber JE: Cyclooxygenase-2 expression correlates with local chronic inflammation and tumor neovascularization in human prostate cancer. Clin Cancer Res. 2005, 11 (9): 3250-3256. 10.1158/1078-0432.CCR-04-2405.CrossRefPubMed Wang W, Bergh A, Damber JE: Cyclooxygenase-2 expression correlates with local chronic inflammation and tumor neovascularization in human prostate cancer. Clin Cancer Res. 2005, 11 (9): 3250-3256. 10.1158/1078-0432.CCR-04-2405.CrossRefPubMed
30.
go back to reference Ghosh AK, Hirasawa N, Niki H, Ohuchi K: Cyclooxygenase-2 mediated angiogenesis in carageenin- induced granulation tissue in rats. J Pharmacol Exp Ther. 2000, 295 (2): 802-809.PubMed Ghosh AK, Hirasawa N, Niki H, Ohuchi K: Cyclooxygenase-2 mediated angiogenesis in carageenin- induced granulation tissue in rats. J Pharmacol Exp Ther. 2000, 295 (2): 802-809.PubMed
31.
32.
go back to reference Stjernschantz J, Nilsson SFE, Astin M: Vasodynamic effects of eicosanoids in the eye. Prog Clin Biol Res. 1989, 312: 155-170.PubMed Stjernschantz J, Nilsson SFE, Astin M: Vasodynamic effects of eicosanoids in the eye. Prog Clin Biol Res. 1989, 312: 155-170.PubMed
33.
go back to reference Cohen T, Nahari D, Cerem LW, Neufeld G, Levi BZ: Interleukin-6 induces the expression of vascular endothelial growth-factor. J Biol Chem. 1996, 271 (2): 736-741. 10.1074/jbc.271.2.736.CrossRefPubMed Cohen T, Nahari D, Cerem LW, Neufeld G, Levi BZ: Interleukin-6 induces the expression of vascular endothelial growth-factor. J Biol Chem. 1996, 271 (2): 736-741. 10.1074/jbc.271.2.736.CrossRefPubMed
34.
go back to reference Ben-Av P, Crofford LJ, Wilder RL, Hla T: Induction of vascular endothelial growth factor expression in synovial fibroblasts by prostaglandin E and interleukin-1: a potential mechanism for inflammatory angiogenesis. FEBS Lett. 1995, 372 (1): 82-87.CrossRef Ben-Av P, Crofford LJ, Wilder RL, Hla T: Induction of vascular endothelial growth factor expression in synovial fibroblasts by prostaglandin E and interleukin-1: a potential mechanism for inflammatory angiogenesis. FEBS Lett. 1995, 372 (1): 82-87.CrossRef
35.
go back to reference Folkman J, Brem H: Angiogenesis and inflammation. Inflammation: basic principles and clinical correlates. Edited by: Gallin JI, Goldstein IM, Snyderman R. 1992, New York: Raven, 821-839. 2 Folkman J, Brem H: Angiogenesis and inflammation. Inflammation: basic principles and clinical correlates. Edited by: Gallin JI, Goldstein IM, Snyderman R. 1992, New York: Raven, 821-839. 2
36.
go back to reference Ayoola GA, Coker HAB, Adesegun SA, Adepoju-Bello AA, Obaweya K, Ezannia EC, Atangbayila TO: Phytochemical screening and antioxidant activites of some selected medicinal plants used for malaria therapy in southwestern Nigeria. Trop J Pharm Res. 2008, 7 (3): 1019-1024. Ayoola GA, Coker HAB, Adesegun SA, Adepoju-Bello AA, Obaweya K, Ezannia EC, Atangbayila TO: Phytochemical screening and antioxidant activites of some selected medicinal plants used for malaria therapy in southwestern Nigeria. Trop J Pharm Res. 2008, 7 (3): 1019-1024.
37.
go back to reference Shelar R, Maurya C, Tekale P, Katkar K, Naik V, Suthar A, Chauhan VS: Embelin - An HPLC Method for Quantitative Estimation in Embelia ribes Burm. F: Int J Pharm Clin Res. 2009, 1 (3): 146-149. Shelar R, Maurya C, Tekale P, Katkar K, Naik V, Suthar A, Chauhan VS: Embelin - An HPLC Method for Quantitative Estimation in Embelia ribes Burm. F: Int J Pharm Clin Res. 2009, 1 (3): 146-149.
38.
go back to reference Veerappan A, Miyazaki S, Kadarkaraisamy M, Ranganathan D: Acute and subacute toxicity studies of Aegle marmelos Corr., an Indian medicinal plant. Phytomedicine. 2007, 14 (2–3): 209-215.CrossRefPubMed Veerappan A, Miyazaki S, Kadarkaraisamy M, Ranganathan D: Acute and subacute toxicity studies of Aegle marmelos Corr., an Indian medicinal plant. Phytomedicine. 2007, 14 (2–3): 209-215.CrossRefPubMed
39.
go back to reference Pakhneshan P, Birsner AE, Adini I, Becker CM, D’Amato R: Differential suppression of vascular permeability and corneal angiogenesis by nonsteroidal anti-inflammatory drugs. Invest Ophthalmol Vis Sci. 2008, 49 (9): 3909-3913. 10.1167/iovs.07-1527.CrossRef Pakhneshan P, Birsner AE, Adini I, Becker CM, D’Amato R: Differential suppression of vascular permeability and corneal angiogenesis by nonsteroidal anti-inflammatory drugs. Invest Ophthalmol Vis Sci. 2008, 49 (9): 3909-3913. 10.1167/iovs.07-1527.CrossRef
40.
go back to reference Wang C, Duan H, He L: Inhibitory effect of atractylenoline I on angiogenesis in chronic inflammation in vivo and in vitro. Eur J Pharmacol. 2009, 612 (1–3): 143-152.CrossRefPubMed Wang C, Duan H, He L: Inhibitory effect of atractylenoline I on angiogenesis in chronic inflammation in vivo and in vitro. Eur J Pharmacol. 2009, 612 (1–3): 143-152.CrossRefPubMed
41.
go back to reference Jackson JR, Bolognese B, Hillegass L, Kassis S, Adams J, Griswold DE, Winkler JD: Pharmacologcal effects of SB 220025, a selective inhibitor of P38 mitogen-activated protein kinasem in angiogenesis and chronic inflammatory disease models. J Pharmacol Exp Ther. 1998, 284 (2): 687-692.PubMed Jackson JR, Bolognese B, Hillegass L, Kassis S, Adams J, Griswold DE, Winkler JD: Pharmacologcal effects of SB 220025, a selective inhibitor of P38 mitogen-activated protein kinasem in angiogenesis and chronic inflammatory disease models. J Pharmacol Exp Ther. 1998, 284 (2): 687-692.PubMed
42.
go back to reference Gonzalez de Mejia E, Ramirez-Mares MV: Ardisia: health-promoting properties and toxicity of phytochemicals and extracts. Toxicol Mech Methods. 2011, 21 (9): 667-674. 10.3109/15376516.2011.601355.CrossRef Gonzalez de Mejia E, Ramirez-Mares MV: Ardisia: health-promoting properties and toxicity of phytochemicals and extracts. Toxicol Mech Methods. 2011, 21 (9): 667-674. 10.3109/15376516.2011.601355.CrossRef
43.
go back to reference Fukuyama Y, Kiriyama Y, Okino J, Kodama M, Iwaki H, Hosozawa S: Naturally occurring 5-lipoxygenase inhibitor. II. Structures and syntheses of ardisianones A and B, and maesanin, alkenyl-1, 4-benzoquinones from the rhizome of Ardisia japonica. Chem Pharm Bull. 1993, 41 (3): 561-565. 10.1248/cpb.41.561.CrossRefPubMed Fukuyama Y, Kiriyama Y, Okino J, Kodama M, Iwaki H, Hosozawa S: Naturally occurring 5-lipoxygenase inhibitor. II. Structures and syntheses of ardisianones A and B, and maesanin, alkenyl-1, 4-benzoquinones from the rhizome of Ardisia japonica. Chem Pharm Bull. 1993, 41 (3): 561-565. 10.1248/cpb.41.561.CrossRefPubMed
44.
go back to reference Fukuyama Y, Kiriyama Y, Okino J, Kodama M, Iwaki H, Hosozawa S: Total synthesis of ardisiaquinone A, a potent 5-lipoxygenase inhibitor, isolated from Ardisia sieboldii, and degree of 5-lipoxygenase inhibitory activity of its derivatives. Chem Pharm Bull. 1994, 42 (10): 2211-2213. 10.1248/cpb.42.2211.CrossRefPubMed Fukuyama Y, Kiriyama Y, Okino J, Kodama M, Iwaki H, Hosozawa S: Total synthesis of ardisiaquinone A, a potent 5-lipoxygenase inhibitor, isolated from Ardisia sieboldii, and degree of 5-lipoxygenase inhibitory activity of its derivatives. Chem Pharm Bull. 1994, 42 (10): 2211-2213. 10.1248/cpb.42.2211.CrossRefPubMed
45.
go back to reference Chang HS, Lin YJ, Lee SJ, Yang CW, Lin WY, Tsai IL, Chen IS: Cytotoxic alkyl benzoquinones and alkyl phenols from Ardisia virens. Phytochemistry. 2009, 70 (17–18): 2064-2071.CrossRefPubMed Chang HS, Lin YJ, Lee SJ, Yang CW, Lin WY, Tsai IL, Chen IS: Cytotoxic alkyl benzoquinones and alkyl phenols from Ardisia virens. Phytochemistry. 2009, 70 (17–18): 2064-2071.CrossRefPubMed
46.
go back to reference Ong CY, Ling SK, Ali RM, Chee CF, Samah ZA, Ho AS, Teo SH, Lee HB: Systematic analysis of in vitro photo-cytotoxic activity to extracts from terrestrial plants in Peninsula Malaysia for photodynamic therapy. J Photochem Photobiol. 2009, 96 (3): 216-222. 10.1016/j.jphotobiol.2009.06.009.CrossRef Ong CY, Ling SK, Ali RM, Chee CF, Samah ZA, Ho AS, Teo SH, Lee HB: Systematic analysis of in vitro photo-cytotoxic activity to extracts from terrestrial plants in Peninsula Malaysia for photodynamic therapy. J Photochem Photobiol. 2009, 96 (3): 216-222. 10.1016/j.jphotobiol.2009.06.009.CrossRef
47.
go back to reference Knighton D, Asprunk D, Tapper D: Avascular and vascular phase of tumor growth in the chick embryo. Br J Cancer. 1977, 35 (3): 347-356. 10.1038/bjc.1977.49.CrossRefPubMedPubMedCentral Knighton D, Asprunk D, Tapper D: Avascular and vascular phase of tumor growth in the chick embryo. Br J Cancer. 1977, 35 (3): 347-356. 10.1038/bjc.1977.49.CrossRefPubMedPubMedCentral
48.
go back to reference Gimbrone MA, Cotran RS, Leapman SB, Folkman J: Tumor growth and neovascularization, an experimental model using rabbit cornea. J Natl Cancer Inst. 1974, 52 (2): 413-427.PubMed Gimbrone MA, Cotran RS, Leapman SB, Folkman J: Tumor growth and neovascularization, an experimental model using rabbit cornea. J Natl Cancer Inst. 1974, 52 (2): 413-427.PubMed
49.
go back to reference Zhang J, Sun Y, Zhang JQ, Ramires FJ, Weber KT: Appearance and regression of rat air pouch tissue. J Mol Cell Cardiol. 1999, 31 (5): 1005-1013. 10.1006/jmcc.1999.0944.CrossRefPubMed Zhang J, Sun Y, Zhang JQ, Ramires FJ, Weber KT: Appearance and regression of rat air pouch tissue. J Mol Cell Cardiol. 1999, 31 (5): 1005-1013. 10.1006/jmcc.1999.0944.CrossRefPubMed
50.
go back to reference Verheul HM, Panigrahy D, Yuan J, D’Amato RJ: Combination oral antiangiogenic therapy with thalidomide and sulindac inhibits tumour growth in rabbits. Br J Cancer. 1999, 79 (1): 114-118. 10.1038/sj.bjc.6690020.CrossRefPubMedPubMedCentral Verheul HM, Panigrahy D, Yuan J, D’Amato RJ: Combination oral antiangiogenic therapy with thalidomide and sulindac inhibits tumour growth in rabbits. Br J Cancer. 1999, 79 (1): 114-118. 10.1038/sj.bjc.6690020.CrossRefPubMedPubMedCentral
51.
go back to reference Senger DR, Van deWater L, Brown LF, Nagy JA, Yeo KT, Yeo TK, Berse B, Jackman RW, Dvorak AM, Dvorak HF: Vascular permeability factor (VPF/VEGF) in tumor biology. Cancer Metastasis Rev. 1993, 12 (3–4): 303-324.CrossRefPubMed Senger DR, Van deWater L, Brown LF, Nagy JA, Yeo KT, Yeo TK, Berse B, Jackman RW, Dvorak AM, Dvorak HF: Vascular permeability factor (VPF/VEGF) in tumor biology. Cancer Metastasis Rev. 1993, 12 (3–4): 303-324.CrossRefPubMed
52.
go back to reference Jennifer AD, Jennifer EH, Gerald EH: Role of apoptosis in anti-angiogenic cancer therapies. Apoptosis, Senescence and Cancer. Edited by: Gewirtz DA, Holt SE, Grant S. 2007, New Jersey: Humana Press Inc, 537-556. Jennifer AD, Jennifer EH, Gerald EH: Role of apoptosis in anti-angiogenic cancer therapies. Apoptosis, Senescence and Cancer. Edited by: Gewirtz DA, Holt SE, Grant S. 2007, New Jersey: Humana Press Inc, 537-556.
53.
go back to reference Chiarugi V, Magnelli L, Gallo O: COX-2, iNOS and p53 as play-makers of tumor angiogenesis. Int J Mol Med. 1998, 2 (6): 715-719.PubMed Chiarugi V, Magnelli L, Gallo O: COX-2, iNOS and p53 as play-makers of tumor angiogenesis. Int J Mol Med. 1998, 2 (6): 715-719.PubMed
54.
go back to reference Vasile E, Qu-Hong , Dvorak HF, Dvorak AM: Caveolae and vesiculo-vacuolar organelles in bovine capillary endothelial cell cultured with VPF/VEGF on floating matrigel-collagen gel. J Histochem Cytochem. 1999, 47 (2): 159-167. 10.1177/002215549904700205.CrossRefPubMed Vasile E, Qu-Hong , Dvorak HF, Dvorak AM: Caveolae and vesiculo-vacuolar organelles in bovine capillary endothelial cell cultured with VPF/VEGF on floating matrigel-collagen gel. J Histochem Cytochem. 1999, 47 (2): 159-167. 10.1177/002215549904700205.CrossRefPubMed
55.
go back to reference Funk CD: Prostaglandins and leukotrienes: Advances in eicosanoids biology. Science. 2001, 294 (5548): 1871-1875. 10.1126/science.294.5548.1871.CrossRefPubMed Funk CD: Prostaglandins and leukotrienes: Advances in eicosanoids biology. Science. 2001, 294 (5548): 1871-1875. 10.1126/science.294.5548.1871.CrossRefPubMed
56.
go back to reference Murohara T, Horowitz JR, Silver M, Tsurumi Y, Chen D, Sullivan A, Isner JM: Vascular endothelial growth factor/vascular permeability factor enhances vascular permeability via nitric oxide and prostacyclin. Circulation. 1998, 97 (1): 99-107. 10.1161/01.CIR.97.1.99.CrossRefPubMed Murohara T, Horowitz JR, Silver M, Tsurumi Y, Chen D, Sullivan A, Isner JM: Vascular endothelial growth factor/vascular permeability factor enhances vascular permeability via nitric oxide and prostacyclin. Circulation. 1998, 97 (1): 99-107. 10.1161/01.CIR.97.1.99.CrossRefPubMed
57.
go back to reference Leahy KM, Koki AT, Masferrer JL: Role of Cyclooxygenases in Angiogenesis. Curr Med Chem. 2000, 7 (11): 1163-1170. 10.2174/0929867003374336.CrossRefPubMed Leahy KM, Koki AT, Masferrer JL: Role of Cyclooxygenases in Angiogenesis. Curr Med Chem. 2000, 7 (11): 1163-1170. 10.2174/0929867003374336.CrossRefPubMed
58.
go back to reference Colville-Nash PR, Alam CA, Appleton I, Browne JR, Seed MP, Willoughby DA: The pharmacological modulation of angiogenesis in chronic granulomatous inflammation. J Pharmacol Exp Ther. 1995, 274 (3): 1463-1472.PubMed Colville-Nash PR, Alam CA, Appleton I, Browne JR, Seed MP, Willoughby DA: The pharmacological modulation of angiogenesis in chronic granulomatous inflammation. J Pharmacol Exp Ther. 1995, 274 (3): 1463-1472.PubMed
59.
go back to reference Gilroy DW, Tomlinson A, Willoughby DA: Differential effects of inhibition of isoforms of cyclooxygenase (COX-1, COX-2) in chronic inflammation. Inflamm Res. 1998, 47 (2): 79-85. 10.1007/s000110050285.CrossRefPubMed Gilroy DW, Tomlinson A, Willoughby DA: Differential effects of inhibition of isoforms of cyclooxygenase (COX-1, COX-2) in chronic inflammation. Inflamm Res. 1998, 47 (2): 79-85. 10.1007/s000110050285.CrossRefPubMed
60.
go back to reference Qu Z, Huang XN, Ahmadi P, Andresevic J, Planck SR, Hart CE, Rosenbaum JT: Expression of basic fibroblast growth factor in synovial tissue from patients with rheumatoid arthritis and degenerative joint disease. Lab Invest. 1995, 73 (3): 339-346.PubMed Qu Z, Huang XN, Ahmadi P, Andresevic J, Planck SR, Hart CE, Rosenbaum JT: Expression of basic fibroblast growth factor in synovial tissue from patients with rheumatoid arthritis and degenerative joint disease. Lab Invest. 1995, 73 (3): 339-346.PubMed
61.
go back to reference Remmers EF, Sano H, Wilder RL: Platelet-derived growth factors and heparin binding (fibroblast) growth factors in the synovial tissue pathology of rheumatoid arthritis. Semin Arthritis Rheum. 1991, 21 (3): 191-199. 10.1016/0049-0172(91)90009-O.CrossRefPubMed Remmers EF, Sano H, Wilder RL: Platelet-derived growth factors and heparin binding (fibroblast) growth factors in the synovial tissue pathology of rheumatoid arthritis. Semin Arthritis Rheum. 1991, 21 (3): 191-199. 10.1016/0049-0172(91)90009-O.CrossRefPubMed
62.
go back to reference Hua H, Feng L, Zhang XP, Zhang LF, Jin J: Anti-angiogenic activity of julibroside J8, a natural product isolated from Albizia julibrissin. Phytomedicine. 1999, 16 (8): 703-711.CrossRef Hua H, Feng L, Zhang XP, Zhang LF, Jin J: Anti-angiogenic activity of julibroside J8, a natural product isolated from Albizia julibrissin. Phytomedicine. 1999, 16 (8): 703-711.CrossRef
Metadata
Title
The hexane fraction of Ardisia crispa Thunb. A. DC. roots inhibits inflammation-induced angiogenesis
Authors
Dayang Erna Zulaikha Awang Hamsin
Roslida Abdul Hamid
Latifah Saiful Yazan
Che Norma Mat Taib
Yeong Looi Ting
Publication date
01-12-2013
Publisher
BioMed Central
Published in
BMC Complementary Medicine and Therapies / Issue 1/2013
Electronic ISSN: 2662-7671
DOI
https://doi.org/10.1186/1472-6882-13-5

Other articles of this Issue 1/2013

BMC Complementary Medicine and Therapies 1/2013 Go to the issue