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Published in: Discover Oncology 4/2012

01-08-2012 | Original Paper

Growth Hormone-Releasing Hormone Receptor Splice Variant 1 is Frequently Expressed in Oral Squamous Cell Carcinomas

Authors: Nikolina Dioufa, Elena Farmaki, Andrew V. Schally, Hippokratis Kiaris, Dimitris Vlahodimitropoulos, Athanasios G. Papavassiliou, Christos Kittas, Norman L. Block, Ioulia Chatzistamou

Published in: Discover Oncology | Issue 4/2012

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Abstract

The expression of growth hormone-releasing hormone (GHRH) splice variant 1 (SV1) receptor in neoplastic lesions of the oral cavity was assessed. The sensitivity of HaCaT keratinocytes to GHRH analogs was also evaluated. Thirty-three benign precancerous oral lesions and 27 squamous cell carcinomas of the oral cavity were evaluated by immunohistochemistry for SV1 expression. SV1 expression in HaCaT keratinocytes was assessed by western blot. HaCaT proliferation was evaluated by cell counting. Anti-SV1 immunoreactivity was detected in only 9  % (three of 33) precancerous lesions (one hyperplasia and two dysplasias), while 44 % (12 of 27) carcinomas were positive for SV1 (p < 0.002). GHRH(1–29)NH2 and GHRH agonist JI-38 stimulated HaCaT proliferation in vitro, and this effect was blocked by GHRH antagonists. These results indicate that SV1 expression may be associated with the transition of precancerous lesions to carcinomas of the oral epithelium. GHRH antagonists may be useful for the management of the disease.
Literature
1.
go back to reference Warnakulasuriya S (2010) Living with oral cancer: epidemiology with particular reference to prevalence and life-style changes that influence survival. Oral Oncol 46(6):407–410PubMedCrossRef Warnakulasuriya S (2010) Living with oral cancer: epidemiology with particular reference to prevalence and life-style changes that influence survival. Oral Oncol 46(6):407–410PubMedCrossRef
2.
go back to reference Lambert R, Sauvaget C, de Camargo CM, Sankaranarayanan R (2011) Epidemiology of cancer from the oral cavity and oropharynx. Eur J Gastroenterol Hepatol 23:633–641PubMedCrossRef Lambert R, Sauvaget C, de Camargo CM, Sankaranarayanan R (2011) Epidemiology of cancer from the oral cavity and oropharynx. Eur J Gastroenterol Hepatol 23:633–641PubMedCrossRef
3.
go back to reference Znaor A, Brennan P, Gajalakshmi V, Mathew A, Shanta V, Varghese C, Boffetta P (2003) Independent and combined effects of tobacco smoking, chewing and alcohol drinking on the risk of oral, pharyngeal and esophageal cancers in Indian men. Int J Cancer 105(5):681–686PubMedCrossRef Znaor A, Brennan P, Gajalakshmi V, Mathew A, Shanta V, Varghese C, Boffetta P (2003) Independent and combined effects of tobacco smoking, chewing and alcohol drinking on the risk of oral, pharyngeal and esophageal cancers in Indian men. Int J Cancer 105(5):681–686PubMedCrossRef
4.
go back to reference Muwonge R, Ramadas K, Sankila R, Thara S, Thomas G, Vinoda J, Sankaranarayanan R (2008) Role of tobacco smoking, chewing and alcohol drinking in the risk of oral cancer in Trivandrum, India: a nested case–control design using incident cancer cases. Oral Oncol 44(5):446–454PubMedCrossRef Muwonge R, Ramadas K, Sankila R, Thara S, Thomas G, Vinoda J, Sankaranarayanan R (2008) Role of tobacco smoking, chewing and alcohol drinking in the risk of oral cancer in Trivandrum, India: a nested case–control design using incident cancer cases. Oral Oncol 44(5):446–454PubMedCrossRef
5.
go back to reference Izumo T (2011) Oral premalignant lesions: from the pathological viewpoint. Int J Clin Oncol 16(1):15–26PubMedCrossRef Izumo T (2011) Oral premalignant lesions: from the pathological viewpoint. Int J Clin Oncol 16(1):15–26PubMedCrossRef
6.
go back to reference Ogmundsdóttir HM, Björnsson J, Holbrook WP (2009) Role of TP53 in the progression of pre-malignant and malignant oral mucosal lesions. A follow-up study of 144 patients. J Oral Pathol Med 38(7):565–571PubMedCrossRef Ogmundsdóttir HM, Björnsson J, Holbrook WP (2009) Role of TP53 in the progression of pre-malignant and malignant oral mucosal lesions. A follow-up study of 144 patients. J Oral Pathol Med 38(7):565–571PubMedCrossRef
7.
go back to reference Sarkis SA, Abdullah BH, Abdul Majeed BA, Talabani NG (2010) Immunohistochemical expression of epidermal growth factor receptor (EGFR) in oral squamous cell carcinoma in relation to proliferation, apoptosis, angiogenesis and lymphangiogenesis. Head Neck Oncol 2:13PubMedCrossRef Sarkis SA, Abdullah BH, Abdul Majeed BA, Talabani NG (2010) Immunohistochemical expression of epidermal growth factor receptor (EGFR) in oral squamous cell carcinoma in relation to proliferation, apoptosis, angiogenesis and lymphangiogenesis. Head Neck Oncol 2:13PubMedCrossRef
8.
go back to reference Taoudi Benchekroun M, Saintigny P, Thomas SM, El-Naggar AK, Papadimitrakopoulou V, Ren H, Lang W, Fan YH, Huang J, Feng L, Lee JJ, Kim ES, Hong WK, Johnson FM, Grandis JR, Mao L (2010) Epidermal growth factor receptor expression and gene copy number in the risk of oral cancer. Cancer Prev Res (Phila) 3(7):800–809CrossRef Taoudi Benchekroun M, Saintigny P, Thomas SM, El-Naggar AK, Papadimitrakopoulou V, Ren H, Lang W, Fan YH, Huang J, Feng L, Lee JJ, Kim ES, Hong WK, Johnson FM, Grandis JR, Mao L (2010) Epidermal growth factor receptor expression and gene copy number in the risk of oral cancer. Cancer Prev Res (Phila) 3(7):800–809CrossRef
9.
go back to reference Bernardes VF, Gleber-Netto FO, Sousa SF, Silva TA, Aguiar MC (2010) Clinical significance of EGFR, Her-2 and EGF in oral squamous cell carcinoma: a case control study. J Exp Clin Cancer Res 29:40PubMedCrossRef Bernardes VF, Gleber-Netto FO, Sousa SF, Silva TA, Aguiar MC (2010) Clinical significance of EGFR, Her-2 and EGF in oral squamous cell carcinoma: a case control study. J Exp Clin Cancer Res 29:40PubMedCrossRef
10.
go back to reference Monteiro LS, Diniz-Freitas M, Garcia-Caballero T, Forteza J, Fraga M (2010) EGFR and Ki-67 expression in oral squamous cell carcinoma using tissue microarray technology. J Oral Pathol Med 39(7):571–578PubMed Monteiro LS, Diniz-Freitas M, Garcia-Caballero T, Forteza J, Fraga M (2010) EGFR and Ki-67 expression in oral squamous cell carcinoma using tissue microarray technology. J Oral Pathol Med 39(7):571–578PubMed
11.
go back to reference Tilakaratne WM, Kobayashi T, Ida-Yonemochi H, Swelam W, Yamazaki M, Mikami T, Alvarado CG, Shahidul AM, Maruyama S, Cheng J, Saku T (2009) Matrix metalloproteinase 7 and perlecan in oral epithelial dysplasia and carcinoma in situ: an aid for histopathologic recognition of their cell proliferation centers. J Oral Pathol Med 38(4):348–355PubMedCrossRef Tilakaratne WM, Kobayashi T, Ida-Yonemochi H, Swelam W, Yamazaki M, Mikami T, Alvarado CG, Shahidul AM, Maruyama S, Cheng J, Saku T (2009) Matrix metalloproteinase 7 and perlecan in oral epithelial dysplasia and carcinoma in situ: an aid for histopathologic recognition of their cell proliferation centers. J Oral Pathol Med 38(4):348–355PubMedCrossRef
12.
go back to reference Thomas GT, Lewis MP, Speight PM (1999) Matrix metalloproteinases and oral cancer. Oral Oncol 35(3):227–233PubMedCrossRef Thomas GT, Lewis MP, Speight PM (1999) Matrix metalloproteinases and oral cancer. Oral Oncol 35(3):227–233PubMedCrossRef
13.
go back to reference Kuo MY, Chang HH, Hahn LJ, Wang JT, Chiang CP (1995) Elevated ras p21 expression in oral premalignant lesions and squamous cell carcinoma in Taiwan. J Oral Pathol Med 24(6):255–260PubMedCrossRef Kuo MY, Chang HH, Hahn LJ, Wang JT, Chiang CP (1995) Elevated ras p21 expression in oral premalignant lesions and squamous cell carcinoma in Taiwan. J Oral Pathol Med 24(6):255–260PubMedCrossRef
14.
go back to reference Kiaris H, Spandidos DA, Jones AS, Vaughan ED, Field JK (1995) Mutations, expression and genomic instability of the H-ras proto-oncogene in squamous cell carcinomas of the head and neck. Br J Cancer 72(1):123–128PubMedCrossRef Kiaris H, Spandidos DA, Jones AS, Vaughan ED, Field JK (1995) Mutations, expression and genomic instability of the H-ras proto-oncogene in squamous cell carcinomas of the head and neck. Br J Cancer 72(1):123–128PubMedCrossRef
15.
go back to reference Kiaris H, Spandidos D, Jones A, Field J (1994) Loss of heterozygosity and microsatellite instability of the H-ras gene in cancer of the head and neck. Int J Oncol 5(3):579–582PubMed Kiaris H, Spandidos D, Jones A, Field J (1994) Loss of heterozygosity and microsatellite instability of the H-ras gene in cancer of the head and neck. Int J Oncol 5(3):579–582PubMed
16.
go back to reference Paterson IC, Eveson JW, Prime SS (1996) Molecular changes in oral cancer may reflect aetiology and ethnic origin. J Cancer B Oral Oncol 32B(3):150–153CrossRef Paterson IC, Eveson JW, Prime SS (1996) Molecular changes in oral cancer may reflect aetiology and ethnic origin. J Cancer B Oral Oncol 32B(3):150–153CrossRef
17.
go back to reference Syrjänen S, Lodi G, von Bültzingslöwen I, Aliko A, Arduino P, Campisi G, Challacombe S, Ficarra G, Flaitz C, Zhou HM, Maeda H, Miller C, Jontell M (2011) Human papillomaviruses in oral carcinoma and oral potentially malignant disorders: a systematic review. Oral Dis 17(Suppl 1):58–72PubMedCrossRef Syrjänen S, Lodi G, von Bültzingslöwen I, Aliko A, Arduino P, Campisi G, Challacombe S, Ficarra G, Flaitz C, Zhou HM, Maeda H, Miller C, Jontell M (2011) Human papillomaviruses in oral carcinoma and oral potentially malignant disorders: a systematic review. Oral Dis 17(Suppl 1):58–72PubMedCrossRef
18.
go back to reference Angiero F, Gatta LB, Seramondi R, Berenzi A, Benetti A, Magistro S, Ordesi P, Grigolato P, Dessy E (2010) Frequency and role of HPV in the progression of epithelial dysplasia to oral cancer. Anticancer Res 30(9):3435–3440PubMed Angiero F, Gatta LB, Seramondi R, Berenzi A, Benetti A, Magistro S, Ordesi P, Grigolato P, Dessy E (2010) Frequency and role of HPV in the progression of epithelial dysplasia to oral cancer. Anticancer Res 30(9):3435–3440PubMed
19.
go back to reference Chatzistamou I, Dioufa N, Trimis G, Sklavounou A, Kittas C, Kiaris H, Papavassiliou AG (2010) p21/waf1 and smooth-muscle actin α expression in stromal fibroblasts of oral cancers. Anal Cell Pathol (Amst) 33(1):19–26 Chatzistamou I, Dioufa N, Trimis G, Sklavounou A, Kittas C, Kiaris H, Papavassiliou AG (2010) p21/waf1 and smooth-muscle actin α expression in stromal fibroblasts of oral cancers. Anal Cell Pathol (Amst) 33(1):19–26
20.
go back to reference Marsh D, Suchak K, Moutasim KA, Vallath S, Hopper C, Jerjes W, Upile T, Kalavrezos N, Violette SM, Weinreb PH, Chester KA, Chana JS, Marshall JF, Hart IR, Hackshaw AK, Piper K, Thomas GJ (2011) Stromal features are predictive of disease mortality in oral cancer patients. J Pathol 223(4):470–481PubMedCrossRef Marsh D, Suchak K, Moutasim KA, Vallath S, Hopper C, Jerjes W, Upile T, Kalavrezos N, Violette SM, Weinreb PH, Chester KA, Chana JS, Marshall JF, Hart IR, Hackshaw AK, Piper K, Thomas GJ (2011) Stromal features are predictive of disease mortality in oral cancer patients. J Pathol 223(4):470–481PubMedCrossRef
21.
go back to reference Meng W, Xia Q, Wu L, Chen S, He X, Zhang L, Gao Q, Zhou H (2011) Downregulation of TGF-beta receptor types II and III in oral squamous cell carcinoma and oral carcinoma-associated fibroblasts. BMC Cancer 11:88PubMedCrossRef Meng W, Xia Q, Wu L, Chen S, He X, Zhang L, Gao Q, Zhou H (2011) Downregulation of TGF-beta receptor types II and III in oral squamous cell carcinoma and oral carcinoma-associated fibroblasts. BMC Cancer 11:88PubMedCrossRef
22.
go back to reference Hiraishi Y, Wada T, Nakatani K, Tojyo I, Matsumoto T, Kiga N, Negoro K, Fujita S (2008) EGFR inhibitor enhances cisplatin sensitivity of oral squamous cell carcinoma cell lines. Pathol Oncol Res 14(1):39–43PubMedCrossRef Hiraishi Y, Wada T, Nakatani K, Tojyo I, Matsumoto T, Kiga N, Negoro K, Fujita S (2008) EGFR inhibitor enhances cisplatin sensitivity of oral squamous cell carcinoma cell lines. Pathol Oncol Res 14(1):39–43PubMedCrossRef
23.
go back to reference Holsinger FC, Doan DD, Jasser SA, Swan EA, Greenberg JS, Schiff BA, Bekele BN, Younes MN, Bucana CD, Fidler IJ, Myers JN (2003) Epidermal growth factor receptor blockade potentiates apoptosis mediated by paclitaxel and leads to prolonged survival in a murine model of oral cancer. Clin Cancer Res 9(8):3183–3189PubMed Holsinger FC, Doan DD, Jasser SA, Swan EA, Greenberg JS, Schiff BA, Bekele BN, Younes MN, Bucana CD, Fidler IJ, Myers JN (2003) Epidermal growth factor receptor blockade potentiates apoptosis mediated by paclitaxel and leads to prolonged survival in a murine model of oral cancer. Clin Cancer Res 9(8):3183–3189PubMed
24.
go back to reference Ludwig B, Ziegler CG, Schally AV, Richter C, Steffen A, Jabs N, Funk RH, Brendel MD, Block NL, Ehrhart-Bornstein M, Bornstein SR (2010) Agonist of growth hormone-releasing hormone as a potential effector for survival and proliferation of pancreatic islets. Proc Natl Acad Sci U S A 107(28):12623–12628PubMedCrossRef Ludwig B, Ziegler CG, Schally AV, Richter C, Steffen A, Jabs N, Funk RH, Brendel MD, Block NL, Ehrhart-Bornstein M, Bornstein SR (2010) Agonist of growth hormone-releasing hormone as a potential effector for survival and proliferation of pancreatic islets. Proc Natl Acad Sci U S A 107(28):12623–12628PubMedCrossRef
25.
go back to reference Kanashiro-Takeuchi RM, Tziomalos K, Takeuchi LM, Treuer AV, Lamirault G, Dulce R, Hurtado M, Song Y, Block NL, Rick F, Klukovits A, Hu Q, Varga JL, Schally AV, Hare JM (2010) Cardioprotective effects of growth hormone-releasing hormone agonist after myocardial infarction. Proc Natl Acad Sci U S A 107(6):2604–2609PubMedCrossRef Kanashiro-Takeuchi RM, Tziomalos K, Takeuchi LM, Treuer AV, Lamirault G, Dulce R, Hurtado M, Song Y, Block NL, Rick F, Klukovits A, Hu Q, Varga JL, Schally AV, Hare JM (2010) Cardioprotective effects of growth hormone-releasing hormone agonist after myocardial infarction. Proc Natl Acad Sci U S A 107(6):2604–2609PubMedCrossRef
26.
go back to reference Granata R, Trovato L, Gallo MP, Destefanis S, Settanni F, Scarlatti F, Brero A, Ramella R, Volante M, Isgaard J, Levi R, Papotti M, Alloatti G, Ghigo E (2009) Growth hormone-releasing hormone promotes survival of cardiac myocytes in vitro and protects against ischaemia–reperfusion injury in rat heart. Cardiovasc Res 83(2):303–312PubMedCrossRef Granata R, Trovato L, Gallo MP, Destefanis S, Settanni F, Scarlatti F, Brero A, Ramella R, Volante M, Isgaard J, Levi R, Papotti M, Alloatti G, Ghigo E (2009) Growth hormone-releasing hormone promotes survival of cardiac myocytes in vitro and protects against ischaemia–reperfusion injury in rat heart. Cardiovasc Res 83(2):303–312PubMedCrossRef
27.
go back to reference Kiaris H, Chatzistamou I, Papavassiliou AG, Schally AV (2011) Growth hormone-releasing hormone: not only a neurohormone. Trends Endocrinol Metab 22:311–317PubMedCrossRef Kiaris H, Chatzistamou I, Papavassiliou AG, Schally AV (2011) Growth hormone-releasing hormone: not only a neurohormone. Trends Endocrinol Metab 22:311–317PubMedCrossRef
28.
go back to reference Schally AV, Varga JL, Engel JB (2008) Antagonists of growth-hormone-releasing hormone: an emerging new therapy for cancer. Nat Clin Pract Endocrinol Metab 4(1):33–43PubMedCrossRef Schally AV, Varga JL, Engel JB (2008) Antagonists of growth-hormone-releasing hormone: an emerging new therapy for cancer. Nat Clin Pract Endocrinol Metab 4(1):33–43PubMedCrossRef
29.
go back to reference Kiaris H, Schally AV, Kalofoutis A (2005) Extrapituitary effects of the growth hormone-releasing hormone. Vitam Horm 70:1–24PubMedCrossRef Kiaris H, Schally AV, Kalofoutis A (2005) Extrapituitary effects of the growth hormone-releasing hormone. Vitam Horm 70:1–24PubMedCrossRef
30.
go back to reference Barabutis N, Schally AV (2010) Growth hormone-releasing hormone: extrapituitary effects in physiology and pathology. Cell Cycle 9(20):4110–4116PubMedCrossRef Barabutis N, Schally AV (2010) Growth hormone-releasing hormone: extrapituitary effects in physiology and pathology. Cell Cycle 9(20):4110–4116PubMedCrossRef
31.
go back to reference Rekasi Z, Czompoly T, Schally AV, Halmos G (2000) Isolation and sequencing of cDNAs for splice variants of growth hormone-releasing hormone receptors from human cancers. Proc Natl Acad Sci U S A 97:10561–10566PubMedCrossRef Rekasi Z, Czompoly T, Schally AV, Halmos G (2000) Isolation and sequencing of cDNAs for splice variants of growth hormone-releasing hormone receptors from human cancers. Proc Natl Acad Sci U S A 97:10561–10566PubMedCrossRef
32.
go back to reference Havt A, Schally AV, Halmos G, Varga JL, Toller GL, Horvath JE, Szepeshazi K, Köster F, Kovitz K, Groot K, Zarandi M, Kanashiro CA (2005) The expression of the pituitary growth hormone-releasing hormone receptor and its splice variants in normal and neoplastic human tissues. Proc Natl Acad Sci U S A 102(48):17424–17429PubMedCrossRef Havt A, Schally AV, Halmos G, Varga JL, Toller GL, Horvath JE, Szepeshazi K, Köster F, Kovitz K, Groot K, Zarandi M, Kanashiro CA (2005) The expression of the pituitary growth hormone-releasing hormone receptor and its splice variants in normal and neoplastic human tissues. Proc Natl Acad Sci U S A 102(48):17424–17429PubMedCrossRef
33.
go back to reference Theophanous E, Petraki C, Scorilas A, Komborozos V, Veloudis G, Varga JL, Zarandi M, Schally AV, Koutsilieris M (2009) The immunohistochemical expression of growth hormone-releasing hormone receptor splice variant 1 is a favorable prognostic marker in colorectal cancer. Mol Med 15(7–8):242–247PubMed Theophanous E, Petraki C, Scorilas A, Komborozos V, Veloudis G, Varga JL, Zarandi M, Schally AV, Koutsilieris M (2009) The immunohistochemical expression of growth hormone-releasing hormone receptor splice variant 1 is a favorable prognostic marker in colorectal cancer. Mol Med 15(7–8):242–247PubMed
34.
go back to reference Köster F, Engel JB, Schally AV, Hönig A, Schröer A, Seitz S, Hohla F, Ortmann O, Diedrich K, Buchholz S (2009) Triple-negative breast cancers express receptors for growth hormone-releasing hormone (GHRH) and respond to GHRH antagonists with growth inhibition. Breast Cancer Res Treat 116(2):273–279PubMedCrossRef Köster F, Engel JB, Schally AV, Hönig A, Schröer A, Seitz S, Hohla F, Ortmann O, Diedrich K, Buchholz S (2009) Triple-negative breast cancers express receptors for growth hormone-releasing hormone (GHRH) and respond to GHRH antagonists with growth inhibition. Breast Cancer Res Treat 116(2):273–279PubMedCrossRef
35.
go back to reference Schulz S, Röcken C, Schulz S (2006) Immunocytochemical localisation of plasma membrane GHRH receptors in human tumours using a novel anti-peptide antibody. Eur J Cancer 42(14):2390–2396PubMedCrossRef Schulz S, Röcken C, Schulz S (2006) Immunocytochemical localisation of plasma membrane GHRH receptors in human tumours using a novel anti-peptide antibody. Eur J Cancer 42(14):2390–2396PubMedCrossRef
36.
go back to reference Chatzistamou I, Volakaki AA, Schally AV, Kiaris H, Kittas C (2008) Expression of growth hormone-releasing hormone receptor splice variant 1 in primary human melanomas. Regul Pept 147(1–3):33–36PubMedCrossRef Chatzistamou I, Volakaki AA, Schally AV, Kiaris H, Kittas C (2008) Expression of growth hormone-releasing hormone receptor splice variant 1 in primary human melanomas. Regul Pept 147(1–3):33–36PubMedCrossRef
37.
go back to reference Kiaris H, Schally AV, Busto R, Halmos G, Artavanis-Tsakonas S, Varga JL (2002) Expression of a splice variant of the receptor for GHRH in 3T3 fibroblasts activates cell proliferation responses to GHRH analogs. Proc Natl Acad Sci U S A 99(1):196–200PubMedCrossRef Kiaris H, Schally AV, Busto R, Halmos G, Artavanis-Tsakonas S, Varga JL (2002) Expression of a splice variant of the receptor for GHRH in 3T3 fibroblasts activates cell proliferation responses to GHRH analogs. Proc Natl Acad Sci U S A 99(1):196–200PubMedCrossRef
38.
go back to reference Kiaris H, Chatzistamou I, Schally AV, Halmos G, Varga JL, Koutselini H, Kalofoutis A (2003) Ligand-dependent and -independent effects of splice variant 1 of growth hormone-releasing hormone receptor. Proc Natl Acad Sci U S A 100(16):9512–9517PubMedCrossRef Kiaris H, Chatzistamou I, Schally AV, Halmos G, Varga JL, Koutselini H, Kalofoutis A (2003) Ligand-dependent and -independent effects of splice variant 1 of growth hormone-releasing hormone receptor. Proc Natl Acad Sci U S A 100(16):9512–9517PubMedCrossRef
39.
go back to reference Barabutis N, Tsellou E, Schally AV, Kouloheri S, Kalofoutis A, Kiaris H (2007) Stimulation of proliferation of MCF-7 breast cancer cells by a transfected splice variant of growth hormone-releasing hormone receptor. Proc Natl Acad Sci U S A 104:5575–5579PubMedCrossRef Barabutis N, Tsellou E, Schally AV, Kouloheri S, Kalofoutis A, Kiaris H (2007) Stimulation of proliferation of MCF-7 breast cancer cells by a transfected splice variant of growth hormone-releasing hormone receptor. Proc Natl Acad Sci U S A 104:5575–5579PubMedCrossRef
40.
go back to reference Izdebski J, Pinski J, Horvath JE, Halmos G, Groot K, Schally AV (1995) Synthesis and biological evaluation of superactive agonists of growth hormone-releasing hormone. Proc Natl Acad Sci U S A 92(11):4872–4876PubMedCrossRef Izdebski J, Pinski J, Horvath JE, Halmos G, Groot K, Schally AV (1995) Synthesis and biological evaluation of superactive agonists of growth hormone-releasing hormone. Proc Natl Acad Sci U S A 92(11):4872–4876PubMedCrossRef
41.
go back to reference Letsch M, Schally AV, Busto R, Bajo AM, Varga JL (2003) Growth hormone-releasing hormone (GHRH) antagonists inhibit the proliferation of androgen-dependent and -independent prostate cancers. Proc Natl Acad Sci U S A 100:1250–1255PubMedCrossRef Letsch M, Schally AV, Busto R, Bajo AM, Varga JL (2003) Growth hormone-releasing hormone (GHRH) antagonists inhibit the proliferation of androgen-dependent and -independent prostate cancers. Proc Natl Acad Sci U S A 100:1250–1255PubMedCrossRef
42.
go back to reference Buchholz S, Schally AV, Engel JB, Hohla F, Heinrich E, Koester F, Varga JL, Halmos G (2007) Potentiation of mammary cancer inhibition by combination of antagonists of growth hormone-releasing hormone with docetaxel. Proc Natl Acad Sci U S A 104(6):1943–1946PubMedCrossRef Buchholz S, Schally AV, Engel JB, Hohla F, Heinrich E, Koester F, Varga JL, Halmos G (2007) Potentiation of mammary cancer inhibition by combination of antagonists of growth hormone-releasing hormone with docetaxel. Proc Natl Acad Sci U S A 104(6):1943–1946PubMedCrossRef
43.
go back to reference Dioufa N, Schally AV, Chatzistamou I, Moustou E, Block NL, Owens GK, Papavassiliou AG, Kiaris H (2010) Acceleration of wound healing by growth hormone-releasing hormone and its agonists. Proc Natl Acad Sci U S A 107(43):18611–18615PubMedCrossRef Dioufa N, Schally AV, Chatzistamou I, Moustou E, Block NL, Owens GK, Papavassiliou AG, Kiaris H (2010) Acceleration of wound healing by growth hormone-releasing hormone and its agonists. Proc Natl Acad Sci U S A 107(43):18611–18615PubMedCrossRef
44.
go back to reference Boukamp P, Petrussevska RT, Breitkreutz D, Hornung J, Markham A, Fusenig NE (1988) Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J Cell Biol 106:761–771PubMedCrossRef Boukamp P, Petrussevska RT, Breitkreutz D, Hornung J, Markham A, Fusenig NE (1988) Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J Cell Biol 106:761–771PubMedCrossRef
Metadata
Title
Growth Hormone-Releasing Hormone Receptor Splice Variant 1 is Frequently Expressed in Oral Squamous Cell Carcinomas
Authors
Nikolina Dioufa
Elena Farmaki
Andrew V. Schally
Hippokratis Kiaris
Dimitris Vlahodimitropoulos
Athanasios G. Papavassiliou
Christos Kittas
Norman L. Block
Ioulia Chatzistamou
Publication date
01-08-2012
Publisher
Springer-Verlag
Published in
Discover Oncology / Issue 4/2012
Print ISSN: 1868-8497
Electronic ISSN: 2730-6011
DOI
https://doi.org/10.1007/s12672-012-0108-8

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