High doses of laser phototherapy can increase proliferation in melanoma stromal connective tissue

  • Lúcio Frigo
  • Joseli Maria Cordeiro
  • Giovani Marino Favero
  • Durnavei Augusto Maria
  • Ernesto Cesar Pinto Leal-Junior
  • Jon Joensen
  • Jan Magnus Bjordal
  • Denise Carvalho Roxo
  • Rodrigo Labat Marcos
  • Rodrigo Alvaro Brandão Lopes-Martins
Original Article
  • 42 Downloads

Abstract

It is well established that laser phototherapy (LP) is contraindicated directly over cancer cells, due to its bio modulatory effects in cell and blood vessel proliferation. The aim of the present study was to analyze the influence of typical low-level laser therapy (LLLT) and high intensity laser therapy (HILT) and an in-between dose of 9 J on collagen fibers and blood vessels content in melanoma tumors (B16F10) implanted in mice. Melanoma tumor cells were injected in male Balb C mice which were distributed in four groups: control (no irradiated) or irradiated by 3, 9, or 21 J (150; 450, or 1050 J/cm2). LP was performed in daily sessions for 3 days with a InGaAlP—660 nm (mean output: 50 mW, spot size: 2 mm2). Tumor volume was analyzed using (1) picrosirius staining to quantify collagen fibers content and (2) Verhoeff’s method to quantify blood vessels content. Tumor growth outcome measured in the 3-J group was not significantly different from controls. Nine and 21-J groups, presented significant and dose-dependent increases in tumor volume. Quantitative analysis of the intensity of collagen fibers and their organization in stroma and peri-tumoral microenvironment showed significant differences between irradiated and control group. Blood vessels count of 21-J group outnumbered the other groups. High doses (≥ 9 J) of LP showed a dose-dependent tumor growth, different collagen fibers characteristics, and eventually blood vessel growth, while a typical LLLT dose (3 J) appeared harmless on melanoma cell activity.

Keywords

Photobiomodulation LLLT Melanoma Collagen Bloob vessels Growing tumor 

Notes

Compliance with ethical standards

Ethical commit

All experiments were carried out in accordance with the guidelines from Cruzeiro do Sul University Bioethical Council for human and animal care, PROTOCOL 011/07.

Conflict of interest

The authors declare that they have no conflict of interest.

Disclaimer

Professor Ernesto Cesar Pinto Leal-Junior received research support from Multi Radiance Medical (Solon, OH), a laser device manufacturer.

Informed consent

All authors agree to the submission of this manuscript.

References

  1. 1.
    Chan HHL, Xiang L, Leung JCK, Tsang KWT, Lai K (2003) In vitro study examining the effect of sub-lethal QS 755 nm lasers on the expression of p16INK4a on melanoma cell lines. Lasers Surg Med 32:88–93CrossRefPubMedGoogle Scholar
  2. 2.
    Kujawa J, Zavodnik IB, Lapshina A, Labieniec M, Bryszewska M (2004) Cell survival, DNA, and protein damage in B14 cells under low-intensity near-infrared (810 nm) laser irradiation. Photomed Laser Surg 22(6):504–508CrossRefPubMedGoogle Scholar
  3. 3.
    Mognato M, Squizzato F, Facchin F, Zaghetto L, Corti L (2004) Cell growth modulation of human cells irradiated in vitro low-level laser therapy. Photomed Laser Surg 22(6):523–526CrossRefPubMedGoogle Scholar
  4. 4.
    de Castro JL, Pinheiro AL, Werneck CE, Soares CP (2005) The effect of laser therapy on the proliferation of oral KB carcinoma cells: an in vitro study. Photomed Laser Surg 23(6):586–589CrossRefPubMedGoogle Scholar
  5. 5.
    Sroka R, Schaffer M, Fuchs C, Pongratz T, Schrader-Reichard U, Busch M, Schaffer PM, Duhmke E, Baumgartner R (1999) Effects on the mitosis of normal and tumor cells induced by light treatment of different wavelengths. Lasers Surg Med 25(3):263–271CrossRefPubMedGoogle Scholar
  6. 6.
    van Leeuwen RL, Dekker SK, Byers HR, Vermeer BJ, Grevelink JM (1996) Modulation of alpha 4 beta 1 and alpha 5 beta 1 integrin expression: heterogeneous effects of Q-switched Ruby, Nd:YAG, and Alexandrite lasers on melanoma cells in vitro. Lasers Surg Med 18(1):63–71CrossRefPubMedGoogle Scholar
  7. 7.
    Zhu NW, Perks CM, Burd AR, Holly JM (1999) Changes in the levels of integrin and focal adhesion kinase (FAK) in human melanoma cells following 532 nm laser treatment. Int J Cancer 82(3):353–358CrossRefPubMedGoogle Scholar
  8. 8.
    Marchesini R, Dasdia T, Melloni E, Rocca E (1989) Effect of low-energy laser irradiation on colony formation capability in different human tumor cells in vitro. Lasers Surg Med 9(1):59–62CrossRefPubMedGoogle Scholar
  9. 9.
    Ocanã-Quero JM, Perez de la Lastra J, Gomez-Villamandos R, Moreno-Millan M (1998) Biological effect of helium-neon (He-Ne) laser irradiation on mouse myeloma (Sp2-Ag14) cell line in vitro. Lasers Med Sci 13:214–218CrossRefGoogle Scholar
  10. 10.
    Jamieson CW, Litwin MS, Longo SE, Krementz ET (1969) Enhancement of melanoma cell culture growth rate by ruby laser radiation. Life Sci 8(2):101–106CrossRefPubMedGoogle Scholar
  11. 11.
    Abe M, Fujisawa K, Suzuki H, Sugimoto T, Kanno T (1993) Role of 830 nm low reactive level laser on the growth of an implanted glioma in mice. Keio J Med 42(4):177–179CrossRefPubMedGoogle Scholar
  12. 12.
    Mester E, Lapis K, Tota JG (1971) Ultrastructural changes in Ehrlich ascites tumor cells following laser irradiation. Arch Geschwulstforsch 38(3):210–220PubMedGoogle Scholar
  13. 13.
    Frigo L, Luppi JSS, Favero GM et al (2009) The effect of low-level laser irradiation (In-Ga-Al-AsP—660 nm) on melanoma in vitro and in vivo. BMC Cancer 9, article 404Google Scholar
  14. 14.
    Lukashev ME, Werb ME (1998) ECM signalling: orchestrating cell behaviour and misbehaviour. Trends Cell Biol 8:437–441CrossRefPubMedGoogle Scholar
  15. 15.
    Mettouchi A, Klein S, Guo W, Lopez-Lago M, Lemichez E, Westwick JK, Giancotti FG (2001) Integrin-specific activation of Rac controls progression through the G(1) phase of the cell cycle. Mol Cell 8:115–127CrossRefPubMedGoogle Scholar
  16. 16.
    Zhao J, Pestell R, Guan JL (2001) Transcriptional activation of cyclin D1 promoter by FAK contributes to cell cycle progression. Mol Biol Cell 12:4066–4077CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Baron-Van Evercooren A, Kleinman HK, Seppä HE, Rentier B, Dubois-Dalcq M (1982) Fibronectin promotes rat Schwann cell growth and motility. J Cell Biol 93(1):211–216CrossRefPubMedGoogle Scholar
  18. 18.
    Vitale M, Illario M, Di Matola T, Casamassima A, Fenzi G, Rossi G (1997) Integrin binding to immobilized collagen and fibronectin stimulates the proliferation of human thyroid cells in culture. Endocrinology 138(4):1642–1648CrossRefPubMedGoogle Scholar
  19. 19.
    Mester E (1966) The use of the laser beam in therapy. Orv Hetil 107(22):1012–1016PubMedGoogle Scholar
  20. 20.
    Medrado AR, Pugliese LS, Reis SR, Andrade ZA (2003) Influence of low level laser therapy on wound healing and its biological action upon myofibroblasts. Lasers Surg Med 32(3):239–244CrossRefPubMedGoogle Scholar
  21. 21.
    Gavish L, Perez L, Gertz SD (2006) Low-level laser irradiation modulates matrix metalloproteinase activity and gene expression in porcine aortic smooth muscle cells. Lasers Surg Med 38(8):779–786CrossRefPubMedGoogle Scholar
  22. 22.
    Choi SK, Kim JH, Lee D, Lee JB, Kim HM, Tchah HW, Hahn TW, Joo M, Ha CI (2008) Different epithelial cleavage planes produced by various epikeratomes in epithelial laser in situ keratomileusis. J Cataract Refract Surg 34(12):2079–2084CrossRefPubMedGoogle Scholar
  23. 23.
    Chen CZ, Raghunath M (2009) Focus on collagen: in vitro systems to study fibrogenesis and antifibrosis state of the art. Fibrogenesis Tissue Repair 2:7CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Yamamoto Y, Kono T, Kotani H, Kasai S, Mito M (1996) Effect of low-power laser irradiation on procollagen synthesis in human fibroblasts. J Clin Laser Med Surg 14(3):129–132PubMedGoogle Scholar
  25. 25.
    Ferreira AN, Silveira L, Genovese WJ, de Araújo VC, Frigo L, de Mesquita RA, Guedes E (2006) Effect of GaAIAs laser on reactional dentinogenesis induction in human teeth. Photomed Laser Surg 24(3):358–365CrossRefPubMedGoogle Scholar
  26. 26.
    Kikuchi T, Maemondo M, Narumi K, Matsumoto K, Nakamura T, Nukiwa T (2002) Tumor suppression induced by intratumor administration of adenovirus vector expressing NK4, a 4-kringle antagonist of hepatocyte growth factor, and naive dendritic cells. Blood 100(12):3950–3959CrossRefPubMedGoogle Scholar
  27. 27.
    Kuwano H, Miyazaki T, Tsutsumi S, Hirayama I, Shimura T, Mochiki E, Nomoto K, Fukuchi M, Kato H, Asao T (2004) Cell density modulates the metastatic aggressiveness of a mouse colon cancer cell line, colon 26. Oncology 67(5–6):441–449CrossRefPubMedGoogle Scholar
  28. 28.
    Rich L, Whittaker P (2005) Collagen and picrosirius red staining: a polarized light assessment of fibrillar hue and spatial distribution. Braz J Morphol Sci 22(2):97–104Google Scholar
  29. 29.
    Barbosa-Júnior AA (2001) Morphological computer-assisted quantitative estimation of stained fibrous tissue in liver sections: applications in diagnosis and experimental research. J Bras Patol 37(3):197–200Google Scholar
  30. 30.
    Coutinho EM et al (1997) Pathogenesis of schistosomal “pipestem” fibrosis (a low-protein diet inhibits the development of “pipestem” fibrosis in mice). Int J Exp Pathol 78:337–342CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Karu TI (1990) Effects of visible radiation on cultured cells. Photochem Photobiol 52:1089–1098CrossRefPubMedGoogle Scholar
  32. 32.
    Liotta LA, Kohn EC (2001) The microenvironment of the tumour–host interface. Nature 411(6835):375–379CrossRefPubMedGoogle Scholar
  33. 33.
    Mueller MM, Fusenig NE (2004) Friends or foes—bipolar effects of the tumour stroma in cancer. Nat Rev Cancer 4(11):839–849CrossRefPubMedGoogle Scholar
  34. 34.
    Tlsty TD, Coussens LM (2006) Tumor stroma and regulation of cancer development. Annu Rev Pathol 1:119–150CrossRefPubMedGoogle Scholar
  35. 35.
    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):263–267CrossRefPubMedGoogle Scholar
  36. 36.
    Ignatieva N, Zakharkina O, Andreeva I, Sobol E, Kamensky V, Lunin V (2008) Effects of laser irradiation on collagen organization in chemically induced degenerative annulus fibrosus of lumbar intervertebral disc. Lasers Surg Med 40(6):422–432CrossRefPubMedGoogle Scholar
  37. 37.
    Prockop D, Kivirikko KI (1995) Collagens: molecular biology, diseases, and potentials for therapy. Annu Rev Biochem 64:403–434CrossRefPubMedGoogle Scholar
  38. 38.
    Yu HS, Chang KL, Yu CL, Chen JW, Chen GS (1996) Low-energy helium-neon laser irradiation stimulates interleukin-1 alpha and interleukin-8 release from cultured human keratinocytes. J Investig Dermatol 107(4):593–596CrossRefPubMedGoogle Scholar
  39. 39.
    Aimbire F, Albertini R, Pacheco MT et al (2006) Low-level laser therapy induces dose-dependent reduction of TNF-alpha levels in acute inflammation. Photomed Laser Surg 24:33–37CrossRefPubMedGoogle Scholar
  40. 40.
    Herz DB, Aitken K, Bagli D (2003) Collagen directly stimulates bladder smooth muscle cell growth in vitro: regulation by extracellular regulated mitogen activated protein kinase. J Urol 170:2072–2076CrossRefPubMedGoogle Scholar
  41. 41.
    Noël A, Jost M, Maquoi E (2008) Matrix metalloproteinases at cancer tumor–host interface. Semin Cell Dev Biol 19(1):52–60 ReviewCrossRefPubMedGoogle Scholar
  42. 42.
    Koyama H, Raines EW, Bornfeldt KE, Roberts JM, Ross R (1996) Fibrillar collagen inhibits arterial smooth muscle proliferation through regulation of Cdk2 inhibitors. Cell 87:1069–1078CrossRefPubMedGoogle Scholar
  43. 43.
    Bacakova L, Wilhel J, Herget J, Novotna J, Eckhart A (1997) Oxidized collagen stimulates proliferation of vascular smooth muscle cells. Exp Mol Pathol 64:185–194CrossRefPubMedGoogle Scholar
  44. 44.
    Henriet P, Zhong ZD, Brooks PC, Weinberg KI, DeClerck YA (2000) Contact with fibrillar collagen inhibits melanoma cell proliferation by up-regulating p27KIP1. Proc Natl Acad Sci U S A 97:10026–10031CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Hagendoorn J, Tong R, Fukumura D, Lin Q, Lobo J, Padera TP, Xu L, Kucherlapati R, Jain RK (2006) Onset of abnormal blood and lymphatic vessel function and interstitial hypertension in early stages of carcinogenesis. Cancer Res 66(7):3360–3364CrossRefPubMedGoogle Scholar
  46. 46.
    Zhang W, Wu C, Pan W, Tian L, Xia J (2004) Low-power Helium-Neon laser irradiation enhances the expression of VEGF in murine myocardium. Chin Med J 117(10):1476–1480PubMedGoogle Scholar
  47. 47.
    Ihsan FR (2005) Low-level laser therapy accelerates collateral circulation and enhances microcirculation. Photomed Laser Surg 23(3):289–294CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag London Ltd., part of Springer Nature 2018

Authors and Affiliations

  • Lúcio Frigo
    • 1
  • Joseli Maria Cordeiro
    • 1
  • Giovani Marino Favero
    • 2
  • Durnavei Augusto Maria
    • 3
  • Ernesto Cesar Pinto Leal-Junior
    • 4
  • Jon Joensen
    • 5
  • Jan Magnus Bjordal
    • 5
    • 6
  • Denise Carvalho Roxo
    • 1
  • Rodrigo Labat Marcos
    • 4
    • 7
  • Rodrigo Alvaro Brandão Lopes-Martins
    • 8
  1. 1.Biological Sciences and Health CenterCruzeiro do Sul UniversitySão PauloBrazil
  2. 2.General Biology DepartmentState University of Ponta GrossaPonta GrossaBrazil
  3. 3.Laboratory of Biochemistry and BiophysicsButantan InstituteSão PauloBrazil
  4. 4.Nove de Julho University (UNINOVE)São PauloBrazil
  5. 5.Institute for PhysiotherapyBergen University CollegeBergenNorway
  6. 6.Physiotherapy Research Group, Department of Global and Public HealthUniversity of BergenBergenNorway
  7. 7.Biophotonics Applied in Health SciencesUniversidade Nove de JulhoSão PauloBrazil
  8. 8.Universidade do Vale do ParaíbaSão José dos CamposBrazil

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