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13-10-2022 | Phototherapy | Original Article

NIR irradiation of human buccal fat pad adipose stem cells and its effect on TRP ion channels

Authors: Leila Gholami, Saeid Afshar, Aliasghar Arkian, Masood Saeidijam, Seyedeh Sareh Hendi, Roghayeh Mahmoudi, Khatereh Khorsandi, Hadi Hashemzehi, Reza Fekrazad

Published in: Lasers in Medical Science | Issue 9/2022

Abstract

The effect of near infrared (NIR) laser irradiation on proliferation and osteogenic differentiation of buccal fat pad-derived stem cells and the role of transient receptor potential (TRP) channels was investigated in the current research. After stem cell isolation, a 940 nm laser with 0.1 W, 3 J/cm² was used in pulsed and continuous mode for irradiation in 3 sessions once every 48 h. The cells were cultured in the following groups: non-osteogenic differentiation medium/primary medium (PM) and osteogenic medium (OM) groups with laser-irradiated (L +), without irradiation (L −), laser treated + Capsazepine inhibitor (L + Cap), and laser treated + Skf96365 inhibitor (L + Skf). Alizarin Red staining and RT-PCR were used to assess osteogenic differentiation and evaluate RUNX2, Osterix, and ALP gene expression levels. The pulsed setting showed the best viability results (P < 0.05) and was used for osteogenic differentiation evaluations. The results of Alizarin red staining were not statistically different between the four groups. Osterix and ALP expression increased in the (L +) group. This upregulation abrogated in the presence of Capsazepine, TRPV1 inhibitor (L + Cap); however, no significant effect was observed with Skf96365 (L + Skf).

Qasim M, Chae DS, Lee NY (2019) Advancements and frontiers in nano-based 3D and 4D scaffolds for bone and cartilage tissue engineering. Int J Nanomed 14:4333–4351. https://doi.org/10.2147/IJN.S209431CrossRef

Aljohani W, Ullah MW, Zhang X, Yang G (2018) Bioprinting and its applications in tissue engineering and regenerative medicine. Int J Biol Macromol 107:261–275. https://doi.org/10.1016/j.ijbiomac.2017.08.171CrossRefPubMed

Alsberg E, Hill EE, Mooney DJ (2001) Craniofacial tissue engineering. Crit Rev Oral Biol Med 12(1):64–75. https://doi.org/10.1177/10454411010120010501CrossRefPubMed

Dzobo K, Thomford NE, Senthebane DA, Shipanga H, Rowe A, Dandara C et al (2018) Advances in regenerative medicine and tissue engineering: innovation and transformation of medicine. Stem Cells International 2018:2495848. https://doi.org/10.1155/2018/2495848CrossRefPubMedPubMedCentral

Tomar GB, Dave J, Chandekar S, Bhattacharya N, Naik S, Kulkarni S et al (2020) Advances in tissue engineering approaches for craniomaxillofacial bone reconstruction. Tissue Engineering and the 5 R's-Reconstruction, Restoration, Replacement, Repair and Regeneration. IntechOpen

Kagami H, Agata H, Tojo A (2011) Bone marrow stromal cells (bone marrow-derived multipotent mesenchymal stromal cells) for bone tissue engineering: basic science to clinical translation. Int J Biochem Cell Biol 43(3):286–289PubMedCrossRef

Sacchetti B, Funari A, Michienzi S, Di Cesare S, Piersanti S, Saggio I et al (2007) Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 131(2):324–336PubMedCrossRef

Shiraishi T, Sumita Y, Wakamastu Y, Nagai K, Asahina I (2012) Formation of engineered bone with adipose stromal cells from buccal fat pad. J Dent Res 91(6):592–597PubMedCrossRef

Fraser JK, Wulur I, Alfonso Z, Hedrick MH (2006) Fat tissue: an underappreciated source of stem cells for biotechnology. Trends Biotechnol 24(4):150–154PubMedCrossRef

10.

Farré-Guasch E, Martí-Pagès C, Hernández-Alfaro F, Klein-Nulend J, Casals N (2010) Buccal fat pad, an oral access source of human adipose stem cells with potential for osteochondral tissue engineering: an in vitro study. Tissue Eng Part C Methods 16(5):1083–1094PubMedCrossRef

11.

Frese L, Dijkman PE, Hoerstrup SP (2016) Adipose tissue-derived stem cells in regenerative medicine. Transfus Med Hemotherapy 43(4):268–274CrossRef

12.

Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ et al (2001) Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7(2):211–228PubMedCrossRef

13.

Takahashi H, Ishikawa H, Tanaka A (2017) Regenerative medicine for Parkinson’s disease using differentiated nerve cells derived from human buccal fat pad stem cells. Hum Cell 30(2):60–71PubMedCrossRef

14.

Kishimoto N, Momota Y, Hashimoto Y, Tatsumi S, Ando K, Omasa T et al (2014) The osteoblastic differentiation ability of human dedifferentiated fat cells is higher than that of adipose stem cells from the buccal fat pad. Clin Oral Invest 18(8):1893–1901CrossRef

15.

Niada S, Ferreira LM, Arrigoni E, Addis A, Campagnol M, Broccaioli E et al (2013) Porcine adipose-derived stem cells from buccal fat pad and subcutaneous adipose tissue for future preclinical studies in oral surgery. Stem Cell Res Ther 4(6):1–11CrossRef

16.

Tsurumachi N, Akita D, Kano K, Matsumoto T, Toriumi T, Kazama T et al (2016) Small buccal fat pad cells have high osteogenic differentiation potential. Tissue Eng Part C Methods 22(3):250–259PubMedCrossRef

17.

Khojasteh A, Sadeghi N (2016) Application of buccal fat pad-derived stem cells in combination with autogenous iliac bone graft in the treatment of maxillomandibular atrophy: a preliminary human study. Int J Oral Maxillofac Surg 45(7):864–871PubMedCrossRef

18.

Khojasteh A, Kheiri L, Behnia H, Tehranchi A, Nazeman P, Nadjmi N et al (2017) Lateral ramus cortical bone plate in alveolar cleft osteoplasty with concomitant use of buccal fat pad derived cells and autogenous bone: phase I clinical trial. BioMed Res Int.

19.

Salehi-Nik N, Rezai Rad M, Kheiri L, Nazeman P, Nadjmi N, Khojasteh A (2017) Buccal fat pad as a potential source of stem cells for bone regeneration: a literature review. Stem Cells Int.

20.

Fossett E, Khan WS (2012) Optimising human mesenchymal stem cell numbers for clinical application: a literature review. Stem Cells Int 2012:465259. https://doi.org/10.1155/2012/465259CrossRefPubMedPubMedCentral

21.

Liesveld JL, Sharma N, Aljitawi OS (2020) Stem cell homing: From physiology to therapeutics. Stem Cells 38(10):1241–1253. https://doi.org/10.1002/stem.3242CrossRefPubMed

22.

Hamblin MR, Demidova TN (2006) Mechanisms of low level light therapy. International Society for Optics and Photonics, Mechanisms for low-light therapyCrossRef

23.

Fekrazad R, Asefi S, Allahdadi M, Kalhori KA (2016) Effect of photobiomodulation on mesenchymal stem cells. Photomed Laser Surg 34(11):533–542PubMedCrossRef

24.

Mvula B, Mathope T, Moore T, Abrahamse H (2008) The effect of low level laser irradiation on adult human adipose derived stem cells. Lasers Med Sci 23(3):277–282PubMedCrossRef

25.

de Villiers JA, Houreld NN, Abrahamse H (2011) Influence of low intensity laser irradiation on isolated human adipose derived stem cells over 72 hours and their differentiation potential into smooth muscle cells using retinoic acid. Stem Cell Rev Rep 7(4):869–882PubMedCrossRef

26.

Ong W-K, Chen H-F, Tsai C-T, Fu Y-J, Wong Y-S, Yen D-J et al (2013) The activation of directional stem cell motility by green light-emitting diode irradiation. Biomaterials 34(8):1911–1920PubMedCrossRef

27.

de Andrade ALM, Luna GF, Brassolatti P, Leite MN, Parisi JR, de Oliveira Leal ÂM et al (2019) Photobiomodulation effect on the proliferation of adipose tissue mesenchymal stem cells. Lasers Med Sci 34(4):677–683PubMedCrossRef

28.

Ginani F, Soares DM, Rocha HADO, Barboza CAG (2017) Low-level laser irradiation promotes proliferation of cryopreserved adipose-derived stem cells. Einstein (São Paulo) 15:334–338PubMedCrossRef

29.

Zare F, Moradi A, Fallahnezhad S, Ghoreishi SK, Amini A, Chien S et al (2019) Photobiomodulation with 630 plus 810 nm wavelengths induce more in vitro cell viability of human adipose stem cells than human bone marrow-derived stem cells. J Photochem Photobiol, B 201:111658PubMedCrossRef

30.

Choi K, Kang BJ, Kim H, Lee S, Bae S, Kweon OK et al (2013) Low-level laser therapy promotes the osteogenic potential of adipose-derived mesenchymal stem cells seeded on an acellular dermal matrix. J Biomed Mater Res B Appl Biomater 101(6):919–928PubMedCrossRef

31.

Abramovitch-Gottlib L, Gross T, Naveh D, Geresh S, Rosenwaks S, Bar I et al (2005) Low level laser irradiation stimulates osteogenic phenotype of mesenchymal stem cells seeded on a three-dimensional biomatrix. Lasers Med Sci 20(3):138–146PubMedCrossRef

32.

Ebrahimpour-Malekshah R, Amini A, Zare F, Mostafavinia A, Davoody S, Deravi N et al (2020) Combined therapy of photobiomodulation and adipose-derived stem cells synergistically improve healing in an ischemic, infected and delayed healing wound model in rats with type 1 diabetes mellitus. BMJ Open Diabetes Res Care 8(1):e001033PubMedPubMedCentralCrossRef

33.

Bayat M, Chien S (2020) Combined adipose-derived mesenchymal stem cells and Photobiomodulation could modulate the inflammatory response and treat infected diabetic foot ulcers, Mary Ann Liebert, Inc., publishers 140 Huguenot Street, 3rd Floor New

34.

Karu TI (2008) Mitochondrial signaling in mammalian cells activated by red and near-IR radiation. Photochem Photobiol 84(5):1091–1099PubMedCrossRef

35.

Karu TI, Kolyakov S (2005) Exact action spectra for cellular responses relevant to phototherapy. Photomed Laser Surg 23(4):355–361PubMedCrossRef

36.

Pastore MG, Passarella SD (2000) Specific helium-neon laser sensitivity of the purified cytochrome c oxidase. Int J Radiat Biol 76(6):863–870PubMedCrossRef

37.

Sommer AP, Schemmer P, Pavláth AE, Försterling H-D, Mester ÁR, Trelles MA (2020) Quantum biology in low level light therapy: death of a dogma. Ann Transl Med 8(7)

38.

Cao E (2020) Structural mechanisms of transient receptor potential ion channels. J Gen Physiol 152(3)

39.

Kaneko Y, Szallasi A (2014) Transient receptor potential (TRP) channels: a clinical perspective. Br J Pharmacol 171(10):2474–2507PubMedPubMedCentralCrossRef

40.

Ogawa N, Kurokawa T, Mori Y (2016) Sensing of redox status by TRP channels. Cell Calcium 60(2):115–122PubMedCrossRef

41.

Cronin MA, Lieu M-H, Tsunoda S (2006) Two stages of light-dependent TRPL-channel translocation in Drosophila photoreceptors. J Cell Sci 119(14):2935–2944PubMedCrossRef

42.

Smani T, Shapovalov G, Skryma R, Prevarskaya N, Rosado JA (2015) Functional and physiopathological implications of TRP channels. Biochimica et Biophysica Acta (BBA)-Mol Cell Res 1853(8):1772–1782

43.

de Freitas LF, Hamblin MR (2016) Proposed mechanisms of photobiomodulation or low-level light therapy. IEEE J Sel Top Quantum Electron 22(3):348–364CrossRef

44.

Hashmi JT, Huang YY, Sharma SK, Kurup DB, De Taboada L, Carroll JD et al (2010) Effect of pulsing in low-level light therapy. Lasers Surg Med 42(6):450–466PubMedPubMedCentralCrossRef

45.

Kim HB, Baik KY, Choung P-H, Chung JH (2017) Pulse frequency dependency of photobiomodulation on the bioenergetic functions of human dental pulp stem cells. Sci Rep 7(1):1–12

46.

Pereira AN, Eduardo Cde P, Matson E, Marques MM (2002) Effect of low-power laser irradiation on cell growth and procollagen synthesis of cultured fibroblasts. Lasers Surg Med 31(4):263–267. https://doi.org/10.1002/lsm.10107CrossRefPubMed

47.

Fiório FB, Albertini R, Leal-Junior EC, de Carvalho Pde T (2014) Effect of low-level laser therapy on types I and III collagen and inflammatory cells in rats with induced third-degree burns. Lasers Med Sci 29(1):313–319. https://doi.org/10.1007/s10103-013-1341-2CrossRefPubMed

48.

Borzabadi-Farahani A (2016) Effect of low-level laser irradiation on proliferation of human dental mesenchymal stem cells; a systemic review. J Photochem Photobiol B 162:577–582. https://doi.org/10.1016/j.jphotobiol.2016.07.022CrossRefPubMed

49.

Mylona V, Anagnostaki E, Chiniforush N, Barikani H, Lynch E, Grootveld M (2022) Photobiomodulation effects on periodontal ligament stem cells: A systematic review of in-vitro studies. Curr Stem Cell Res Ther. https://doi.org/10.2174/1574888x17666220527090321CrossRefPubMed

50.

Choi EJ, Yim JY, Koo KT, Seol YJ, Lee YM, Ku Y et al (2010) Biological effects of a semiconductor diode laser on human periodontal ligament fibroblasts. J Periodontal Implant Sci 40(3):105–110. https://doi.org/10.5051/jpis.2010.40.3.105CrossRefPubMedPubMedCentral

51.

Wang Y, Huang YY, Wang Y, Lyu P, Hamblin MR (2017) Photobiomodulation of human adipose-derived stem cells using 810nm and 980nm lasers operates via different mechanisms of action. Biochim Biophys Acta Gen Subj 1861(2):441–449. https://doi.org/10.1016/j.bbagen.2016.10.008CrossRefPubMed

52.

Huang Y-Y, Sharma SK, Carroll J, Hamblin MR (2011) Biphasic dose response in low level light therapy—an update. Dose-Response 9(4): dose-response. 11–009. Hamblin

53.

Cheng K, Martin LF, Slepian MJ, Patwardhan AM, Ibrahim MM (2021) Mechanisms and pathways of pain photobiomodulation: a narrative review. J Pain

54.

Dompe C, Moncrieff L, Matys J, Grzech-Leśniak K, Kocherova I, Bryja A et al (2020) Photobiomodulation—underlying mechanism and clinical applications. J Clin Med 9(6):1724PubMedPubMedCentralCrossRef

55.

Jawad MM, Husein A, Azlina A, Alam MK, Hassan R, Shaari R (2013) Effect of 940 nm low-level laser therapy on osteogenesis in vitro. J Biomed Opt 18(12):128001PubMedCrossRef

56.

Huertas RM, Luna-Bertos ED, Ramos-Torrecillas J, Leyva FM, Ruiz C, García-Martínez O (2014) Effect and clinical implications of the low-energy diode laser on bone cell proliferation. Biol Res Nurs 16(2):191–196PubMedCrossRef

57.

Santana-Blank LA, Rodríguez-Santana E, Santana-Rodríguez KE (2005) Photo-infrared pulsed bio-modulation (PIPBM): a novel mechanism for the enhancement of physiologically reparative responses. Photomed Laser Ther 23(4):416–424CrossRef

58.

Chung H, Dai T, Sharma SK, Huang YY, Carroll JD, Hamblin MR (2012) The nuts and bolts of low-level laser (light) therapy. Ann Biomed Eng 40(2):516–533. https://doi.org/10.1007/s10439-011-0454-7CrossRefPubMed

59.

Joensen J, Ovsthus K, Reed RK, Hummelsund S, Iversen VV, Lopes-Martins R et al (2012) Skin penetration time-profiles for continuous 810 nm and superpulsed 904 nm lasers in a rat model. Photomed Laser Surg 30(12):688–694. https://doi.org/10.1089/pho.2012.3306CrossRefPubMed

60.

Kim HB, Baik KY, Choung PH, Chung JH (2017) Pulse frequency dependency of photobiomodulation on the bioenergetic functions of human dental pulp stem cells. Sci Rep 7(1):15927. https://doi.org/10.1038/s41598-017-15754-2CrossRefPubMedPubMedCentral

61.

Marques NP, Lopes CS, Marques NCT, Cosme-Silva L, Oliveira TM, Duque C et al (2019) A preliminary comparison between the effects of red and infrared laser irradiation on viability and proliferation of SHED. Lasers Med Sci 34(3):465–471. https://doi.org/10.1007/s10103-018-2615-5CrossRefPubMed

62.

Ladiz MAR, Mirzaei A, Hendi SS, Najafi-Vosough R, Hooshyarfard A, Gholami L (2020) Effect of photobiomodulation with 810 and 940 nm diode lasers on human gingival fibroblasts. Dent Med Probl 57(4):369–376. https://doi.org/10.17219/dmp/122688CrossRefPubMed

63.

Keshri GK, Gupta A, Yadav A, Sharma SK, Singh SB (2016) Photobiomodulation with pulsed and continuous wave near-infrared laser (810 nm, Al-Ga-As) augments dermal wound healing in immunosuppressed rats. PLoS One 11(11):e0166705PubMedPubMedCentralCrossRef

64.

Ando T, Xuan W, Xu T, Dai T, Sharma SK, Kharkwal GB et al (2011) Comparison of therapeutic effects between pulsed and continuous wave 810-nm wavelength laser irradiation for traumatic brain injury in mice. PLoS One 6(10):e26212PubMedPubMedCentralCrossRef

65.

Lapchak PA, Salgado KF, Chao CH, Zivin JA (2007) Transcranial near-infrared light therapy improves motor function following embolic strokes in rabbits: an extended therapeutic window study using continuous and pulse frequency delivery modes. Neuroscience 148(4):907–914. https://doi.org/10.1016/j.neuroscience.2007.07.002CrossRefPubMed

66.

Bayat M, Azari A, Golmohammadi MG (2010) Effects of 780-nm low-level laser therapy with a pulsed gallium aluminum arsenide laser on the healing of a surgically induced open skin wound of rat. Photomed Laser Surg 28(4):465–470PubMedCrossRef

67.

AlWattar WM (2021) Effect of low energy laser on the healing of tooth extraction wound:(Histological Study in Rat). Iraqi J Laser 20(1):30–38

68.

Ueda Y, Shimizu N (2003) Effects of pulse frequency of low-level laser therapy (LLLT) on bone nodule formation in rat calvarial cells. J Clin Laser Med Surg 21(5):271–277PubMedCrossRef

69.

Bruderer M, Richards R, Alini M, Stoddart MJ (2014) Role and regulation of RUNX2 in osteogenesis. Eur Cell Mater 28(28):269–286PubMedCrossRef

70.

Hoemann C, El-Gabalawy H, McKee M (2009) In vitro osteogenesis assays: influence of the primary cell source on alkaline phosphatase activity and mineralization. Pathol Biol 57(4):318–323PubMedCrossRef

71.

Komori T (2003) Requisite roles of Runx2 and Cbfb in skeletal development. J Bone Miner Metab 21(4):193–197PubMed

72.

Nakashima K, Zhou X, Kunkel G, Zhang Z, Deng JM, Behringer RR et al (2002) The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell 108(1):17–29PubMedCrossRef

73.

Artigas N, Ureña C, Rodríguez-Carballo E, Rosa JL, Ventura F (2014) Mitogen-activated protein kinase (MAPK)-regulated interactions between Osterix and Runx2 are critical for the transcriptional osteogenic program. J Biol Chem 289(39):27105–27117PubMedPubMedCentralCrossRef

74.

Ortuño MJ, Ruiz-Gaspà S, Rodríguez-Carballo E, Susperregui AR, Bartrons R, Rosa JL et al (2010) p38 regulates expression of osteoblast-specific genes by phosphorylation of osterix. J Biol Chem 285(42):31985–31994PubMedPubMedCentralCrossRef

75.

Nilius B, Owsianik G (2011) The transient receptor potential family of ion channels. Genome Biol 12(3):1–11CrossRef

76.

Marwaha L, Bansal Y, Singh R, Saroj P, Bhandari R, Kuhad A (2016) TRP channels: potential drug target for neuropathic pain. Inflammopharmacology 24(6):305–317PubMedCrossRef

77.

Hamblin MR (2016) Shining light on the head: photobiomodulation for brain disorders. BBA clinical 6:113–124PubMedPubMedCentralCrossRef

78.

Levine JD, Alessandri-Haber N (2007) TRP channels: targets for the relief of pain. Biochimica et Biophysica Acta (BBA)-Mol Basis Dis 1772(8):989–1003.

79.

Wang Y, Huang Y-Y, Wang Y, Lyu P, Hamblin MR (2017) Photobiomodulation of human adipose-derived stem cells using 810 nm and 980 nm lasers operates via different mechanisms of action. Biochimica et Biophysica Acta (BBA)-Gen Subj 1861(2):441–449

80.

Wang Y, Huang Y-Y, Wang Y, Lyu P, Hamblin MR (2016) Photobiomodulation (blue and green light) encourages osteoblastic-differentiation of human adipose-derived stem cells: role of intracellular calcium and light-gated ion channels. Sci Rep 6(1):1–9

81.

Gutknecht N, Franzen R, Schippers M, Lampert F (2004) Bactericidal effect of a 980-nm diode laser in the root canal wall dentin of bovine teeth. J Clin Laser Med Surg 22(1):9–13PubMedCrossRef

82.

Kawagishi-Hotta M, Hasegawa S, Igarashi T, Yamada T, Takahashi M, Numata S et al (2017) Enhancement of individual differences in proliferation and differentiation potentials of aged human adipose-derived stem cells. Regen Ther 6:29–40. https://doi.org/10.1016/j.reth.2016.12.004CrossRefPubMedPubMedCentral

83.

Juntunen M, Heinonen S, Huhtala H, Rissanen A, Kaprio J, Kuismanen K et al (2021) Evaluation of the effect of donor weight on adipose stromal/stem cell characteristics by using weight-discordant monozygotic twin pairs. Stem Cell Res Ther 12(1):516. https://doi.org/10.1186/s13287-021-02587-0CrossRefPubMedPubMedCentral

84.

Payr S, Schuseil T, Unger M, Seeliger C, Tiefenboeck T, Balmayor ER et al (2020) Effect of donor age and 3D-cultivation on osteogenic differentiation capacity of adipose-derived mesenchymal stem cells. Sci Rep 10(1):10408. https://doi.org/10.1038/s41598-020-67254-5CrossRefPubMedPubMedCentral

Title: NIR irradiation of human buccal fat pad adipose stem cells and its effect on TRP ion channels
Authors: Leila Gholami
Saeid Afshar
Aliasghar Arkian
Masood Saeidijam
Seyedeh Sareh Hendi
Roghayeh Mahmoudi
Khatereh Khorsandi
Hadi Hashemzehi
Reza Fekrazad
Publication date: 13-10-2022
Publisher: Springer London
Keywords: Phototherapy
Laser
Published in: Lasers in Medical Science / Issue 9/2022
Print ISSN: 0268-8921
Electronic ISSN: 1435-604X
DOI: https://doi.org/10.1007/s10103-022-03652-7

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NIR irradiation of human buccal fat pad adipose stem cells and its effect on TRP ion channels

Abstract

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