In Vitro Action of Matrix Metalloproteinases 2 and 9 Inhibitors on Na+/K+-ATPase, H+/K+-ATPase and PMCA Activities in the Osmoregulatory Epithelia of Climbing Perch (Anabas testudineus Bloch)
Authors
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Department of Zoology, University of Kerala, Kariavattom, Thiruvananthapuram– 695581, Kerala ,IN
G. S. Sheetal -
Inter-University Centre for Evolutionary and Integrative Biology (iCEIB), School of Life Sciences, University of Kerala, Kariavattom, Thiruvananthapuram– 695581, Kerala ,INValsa S. Peter
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Inter-University Centre for Evolutionary and Integrative Biology (iCEIB), School of Life Sciences, University of Kerala, Kariavattom, Thiruvananthapuram– 695581, Kerala ,INM. C. Subhash Peter
DOI:
https://doi.org/10.18311/jer/2018/24711Keywords:
MMP, fish, ECM, Na / K -ATPase, PMCA, H /K -ATPase, Metalloproteinase, Anabas testudineusAbstract
Matrix metalloproteinases 2 and 9 (MMP2 and MMP9) are involved in the extracellular matrix (ECM) remodeling. We tested the short-term in vitro action of inhibitors of MMP2 and MMP9 on P-type ion transporter function in organ explants of climbing perch (Anabas testudineus) to understand how these ECM remodeling components influence the ion transporter function in the osmoregulatory epithelia of fish. Graded doses (10-8, 10-7 and 10-6 M) of inhibitors of MMP2 and MMP9 were administered in vitro to explants of gills, kidney and intestine, kept for either 15 or 30 min and the activities of P-type ATPase such as Na+/K+-ATPase (NKA), H+/K+-ATPase (HKA) and plasma membrane Ca2+-ATPase (PMCA) were quantified. We found that the inhibitors of MMP2 and MMP9 produced dose- and time-dependent modulation in the activities of NKA, HKA and PMCA in the tested tissue explants. Incubation of MMP2 and 9 inhibitors at the highest dose (10-6 M) for 15 and 30 min produced substantial rise in NKA activity. Likewise, HKA activity that showed significant rise after incubation of 10-7 and 10-8 M inhibitors in gills and kidney explants, decreased at the lowest dose (10-8 M) of inhibitors. The lower doses of both inhibitors, while increasing PMCA activity in kidney and intestinal explants inhibited its activity in gill explant. These differential tissue-responsive actions of MMP2 and MMP9 inhibitors indicate that these ECM remodeling components can modify the function of the membrane-bound P-type ion transporters in the osmoregulatory tissues of fish.
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Wang S, Sekekuchi R, Daley WP, Yamada KM. Patterned cell and matrix dynamics in branching morphogenesis. J Cell Biol. 2017; 216(3):559–70.
Govindan J, Iovine MK. Dynamic remodeling of the extracellular matrix during zebrafish fin regeneration. Gene Expr. Patterns. 2015; 19(1-2):1–9.
Ruiz PA, Jarai G. Discoidin domain receptors regulate the migration of primary human lung fibroblasts through collagen matrices. Fibrogenesis Tissue Repair. 2013; 5(3):1–9.
Stamenkovic I. Extracellular matrix remodelling: the role of matrix metalloproteinases. J. Pathol. 2003; 200(4):448–64.
Alberts B, Johnson A, Lewis J et al. Molecular Biology of the Cell. New York, London: Garland Science; 2007.
Schaefer L. Proteoglycans, key regulators of cell-matrix dynamics. Matrix Biol. 2014; 35:1–2.
Egeblad M, Rasch MG, Weaver VM. Dynamic interplay between the collagen scaffold and tumor evolution. Curr Opin Cell Biol. 2010; 22(5):697–706.
Hubmacher D, Apte SS. The biology of the extracellular matrix: novel insights. Curr Opin Rheumatol. 2013; 25(1):65–70.
Mott JD, Werb Z. Regulation of matrix biology by matrix metalloproteinases. Curr Opin Cell Biol. 2004;16(5):558–64.
Werb Z. ECM and cell surface proteolysis: regulating cellular ecology. Cell. 1997; 91(4):439–42.
Marecko I, Cvejic D, Selemetjev S, et al. Enhanced activation of matrix metalloproteinase-9 correlates with the degree of papillary thyroid carcinoma infiltration. Croat Med J. 2014; 55(2):128–37.
Sternlicht MD, Werb Z. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol. 2001; 17:463–516.
Bjorkulund M, Koivunen E. Gelatinase-mediated migration and invasion of cancer cells. Biochem Biophys Acta. 2005; 1755(1):37–69.
Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell. 2010; 141(1):52–67.
Trocme C, Gaudin P, Berthier S, et al. Human B lymphocytes synthesize the 92-kDa gelatinase, matrix metalloproteinase9. J Biol Chem. 1998: 273:20677–84.
Munaut C, Salonurmi T, Kontusaari S, et al. Murine matrix metalloproteinase 9 Gene. J Biol Chem. 1999; 274(9):5588–96.
Marshall WS, Howard JA, Cozzi RRF, Lynch EM. NaCl and fluid secretion by the intestine of the teleost Fundulus heteroclitus: involvement of CFTR. J Exp Biol. 2002; 205:745–58.
Evans DH. Teleost fish osmoregulation : what have we learned since August Krogh, Homer Smith, and Ancel Keys. Am J Physiol Regul Integr Comp Physiol.2008; 295(2):704–13.
Babitha GS, Peter MCS. Cortisol promotes and integrates the osmotic competence of the organs in North African catfish (Clarias gariepinus Burchell): Evidence from in vivo and in situ approaches. Gen Comp Endocrinol. 2010; 168(1):14–21.
Wilfred D, Peter VS, Peter MCS. Rapid in situ action of estradiol 17β on ion transporter function in brain segments of female Mozambique tilapia (Oreochromis mossambicus Peters). J Endocrinol Repr. 2017; 21(2):59–66.
Simi S, Peter VS, Peter MCS. Zymosan-induced immune challenge modifies the stress response of hypoxic air-breathing fish (Anabas testudineus Bloch): Evidence for reversed patterns of cortisol and thyroid hormone interaction, differential ion transporter functions and non-specific immune response. Gen Comp Endocrinol. 2017; 251:94–108.
Kaplan JH, Ase K. Biochemistry of Na,K-ATPase. Annu Rev Biochem. 2002; 71:511–535.
Karlish JDS, Tal D, Katz A, Kapri-Pardes E, et al. The sodium-potassium pump: structure, function, regulation and pharmacology. Life Science Open Day. Weizmann Institute of Science. 2008.
Morth JP, Pedersen BP, Toustrup-jensen MS, et al. Crystal structure of the sodium – potassium pump. Nature. 2007; 450:1043–50.
Poulsen H, Morth P, Egebjerg J, Nissen P. Phosphorylation of the Na+, K+-ATPase and the H+, K+-ATPase. FEBS Lett. 2010; 584:2589–95.
Schwab BL, Guerini D, Didszun C, et al. Cleavage of plasma membrane calcium pumps by caspases: a link between apoptosis and necrosis. Cell Death Differ. 2002; 9:818–31.
Orrenius S, Zhivotovsky B, Nicotera P. Regulation of cell death: the calcium – apoptosis link. Nat Rev Mol Cell Biol. 2003; 4:552–65.
Brini M, Carafoli E. The plasma membrane Ca2+ ATPase and the plasma membrane sodium calcium exchanger cooperate in the regulation of cell calcium. Cold Spring Harb Perspect Biol. 2011; 3:1–15.
Pedersen ME, Vuong TT, Ronning SB, Kolset SO. Matrix metalloproteinases in fish biology and matrix turnover. Matrix Biol. 2015; 44:86–93.
Lodemel JB, Olsen RL. Gelatinolytic activities in muscle of Atlantic cod (Gadus morhua), spotted wolffish (Anarhichas minor) and Atlantic salmon (Salmo salar) J Sci Food Agric. 2003; 83:1031–36.
Bai S, Thummel R, Godwin AR, et al. Matrix metalloproteinase expression and function during fin regeneration in zebrafish : Analysis of MT1-MMP, MMP2 and TIMP2 B. Matrix Biol. 2005; 24:247–260.
Castillo-brice P, Arizcun-arizcun M, Meseguer J. Correlated expression profile of extracellular matrix-related molecules during the inflammatory response of the teleost fish gilthead seabream. Dev Comp Immunol. 2010; 34:1051–58.
McCormick SD. The hormonal control of osmoregulation in teleost fish. In: Farrell AP, (ed.), Encyclopedia of Fish Physiology: From Genome to Environment, 2011; 2: 1466–73.
Jiang Y, Abernathy JW, Peatman E, et al. Identification and characterization of matrix metalloproteinase-13 sequence structure and expression during embryogenesis and infection in channel catfish (Ictalurus punctatus). Dev Comp Immunol. 2010; 34:590–597.
Volkman HE, Pozos TC, Zheng J, et al. Tuberculous granuloma induction via interaction of a bacterial secreted protein with host epithelium. Science. 2010; 327:466–9.
Vrieze ED, Sharif F, Metz JR, Flik G, Richardson MK. Matrix metalloproteinases in osteoclasts of ontogenetic and regenerating zebrafish scales. Bone. 2011; 48:704–12.
Bonventre JA, White LA, Cooper KR. Craniofacial abnormalities and altered wnt and MMP mRNA expression in zebrafish embryos exposed to gasoline oxygenates ETBE and TAME. Aquat Toxicol. 2015; 15:45–53.
Talwar PK, Jhingran AG. Inland Fishes of India and Adjacent Countries. Oxford and IBH Publishing: New Delhi, India; 1991; 1:1158.
Peter MCS. Thyroid Hormones and Hydromineral Regulation during Stress in Fish, D.Sc. thesis, Radboud University Nijmegen, The Netherlands. 2007.
Peter MCS, Leji J, Peter VS. Ambient salinity modifies the action of triiodothyronine in the air-breathing fish Anabas testudineus Bloch: Effects on mitochondria-rich cell distribution, osmotic and metabolic regulations. Gen Comp Endocrinol. 2011; 171:225–31.
Alexander JB, Ingram GA. A comparison of five methods commonly used to measure protein concentration of fish sera. J Fish Biol. 1980; 16:115–22.
Stamenkovic I, Bosman FT. Functional structure and composition of the extracellular matrix. J Pathol. 2003; 200: 423–28.
Iren A, Stanca L, Sima C, et al. Chemico-biological interactions complex responses to Si quantum dots accumulation in carp liver tissue: Beyond oxidative stress. Chem Biol Interact. 2015; 239:56–66.
Matrisian LM. The matrix-degrading metalloproteinases. Bioessays. 1992; 14:455–63.
Woessner JF. The family of matrix metalloproteinases. Ann NY Acad Sci. 1994; 732:11–21.
Stetler-Stevenson WG. Commentary dynamics of matrix turnover during pathologic remodeling of the extracellular matrix. Am J Pathol. 1996; 148:1345–50.
Evans DH, Claiborne JB. The Physiology of Fishes. Taylor and Francis, 3rd edition. 2015; 601 p:319–42.
Polette MP, Uet EH, Irembaut PB, et al. Influence of oleic acid on the expression, activation and activity of gelatinase a produced by oncogene-transformed human bronchial epithelial cells. Int J Cancer. 1999; 80:751–5.
Sato H, Takino T, Okada Y, et al. Matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature. 1994; 70:61–5.
McCormick SD. Endocrine control of osmoregulation in teleost fish. Am Zool. 2001; 41; 781-794.
Peter MCS. Understanding the adaptive response in vertebrates: The phenomenon of ease and ease response during post-stress acclimation. Gen Comp Endocrinol. 2013; 181: 59–64.
Hirose S, Kaneko T, Naito N, Takei Y. Molecular biology of major components of chloride cells. Comp Biochem Physiol B Biochem Mol Biol. 2003; 136:593–620.
Bobulescu IA, Moe OW. Luminal Na+/H+ exchange in the proximal tubule. Eur J Physiol. 2008; 458:5–21.
Lorin-nebel C, Boulo V, Bodinier C, Charmantier G. Na+ / K + / 2Cl – cotransporter in the sea bass Dicentrarchus labrax during ontogeny: involvement in osmoregulation. J Exp Biol. 2006; 209:4908–22.
Rajagopal M, Wallace DP. Chloride secretion by renal collecting ducts. Curr Opin Nephrol Hypertens. 2015; 24:444–9.
Kimura A, Shinohara M, Ohkura R, Takahashi T. Expression and localization of transcripts of MT5-MMP and its related MMP in the ovary of the medaka fish Oryzias latipes. Biochim Biophys Acta – Gene Struct. 2001; 1518:115–23.
Zhang J, Bai S, Tanase C, et al. The expression of tissue inhibitor of metalloproteinase 2 (TIMP-2) is required for normal development of zebrafish embryos. Dev Genes Evol. 2003; 213:382–9.
Hillegass JM, Villano CM, Cooper KR, White LA. Matrix metalloproteinase-13 is required for zebrafish (Danio rerio) development and is a target for glucocorticoids. Toxicol Sci. 2007; 100:168–79.
Chadzinska M, Baginski P, Huub FJ, Lidy BM. Expression profiles of matrix metalloproteinase 9 in teleost fish provide evidence for its active role in initiation and resolution of inflammation. J immunol. 2008; 125:601–10.
Williams TM, Medina F, Badano I, et al. Caveolin-1 gene disruption promotes mammary tumorigenesis and dramatically enhances lung metastasis in vivo. J Biol Chem. 2004; 279:51630-46.
Tholozan FMD, Gribbon C, Li Z, et al. FGF-2 release from the lens capsule by MMP-2 maintains lens epithelial cell viability. Mol Biol Cell. 2007; 18:4222–31.
Karakiulakis G, Papakonstantinou E., Aletras AJ, et al. Cell type-specific effect of hypoxia and platelet-derived growth factor-BB on extracellular matrix turnover and its consequences for lung remodeling. J Biol Chem. 2007; 282: 908–15.
Wang Z, Kong L, Kang J, et al. Thrombin stimulates mitogenesis in pig cerebrovascular smooth muscle cells involving activation of pro-matrix metalloproteinase-2. Neurosci Lett. 2003; 451:199–203.
Sun HJ, Zhao MX, Ren XS, et al. Salusin-β promotes vasculars muscle cell migration and intimal hyperplasia after vascular injury via ROS/NFκB/MMP-9 pathway. Antioxid Redox Signal. 2016; 18:1045–57.
An J, Xue Y, Long M, et al. Targeting CCR2 with its antagonist suppresses viability, motility and invasion by downregulating MMP-9 expression in non-small cell lung cancer cells. Oncotarget. 2017; 8:39230–40.
Moyle PB, Cech JJ. Hydromineral balance. Fishes, An Introduction to Ichthyology. 2000; 8:79–96.
Sakai H, Fujii T, Takeguchi N. Proton-potassium (H+/K+) ATPases: Properties and roles in health and diseases. In: Sigel A., Sigel H., Sigel R. (eds) The Alkali Metal Ions: Their Role for Life. Metal Ions in Life Sciences, 2016; 16.
Jorgensen PL, Hakansson KO, Karlish SJ. Structure and mechanism of Na,K-ATPase: functional sites and their interactions. Annu Rev Physiol. 2002; 65:817–49.
Schwab A, Fabian A, Hanley PJ, Stock C. Mechanisms of cell migration. Physiol Rev. 2012; 92:1865–913.
