Insulin-like growth factor 1 triggers salt secretion machinery in fish under acute salinity stress

in Journal of Endocrinology
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  • 1 Institute of Cellular and Organismic Biology, Academica Sincia, Taipei, Taiwan, Republic of China

Correspondence should be addressed to P-P Hwang: pphwang@gate.sinica.edu.tw
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Timely adjustment of osmoregulation upon acute salinity stress is essential for the survival of euryhaline fish. This rapid response is thought to be tightly controlled by hormones; however, there are still questions unanswered. In this work, we tested the hypothesis that the endocrine hormone, insulin-like growth factor 1 (Igf1), a slow-acting hormone, is involved in the activation of salt secretion mechanisms in euryhaline medaka (Oryzias melastigma) during acclimation to acute salinity stress. In response to a 30-ppt seawater (SW) challenge, Na+/Cl secretion was enhanced within 0.5 h, with concomitant organization of ionocyte multicellular complexes and without changes in expression of major transporters. Igf1 receptor inhibitors significantly impair the Na+/Cl secretion and ionocyte multicellular complex responses without affecting transporter expression. Thus, Igf1 may activate salt secretion as part of the teleost response to acute salinity stress by exerting effects on transporter function and enhancing the formation of ionocyte multicellular complexes. These findings provide new insights into hormonal control of body fluid ionic/osmotic homeostasis during vertebrate evolution.

Supplementary Materials

    • Supplementary Table 1. Sequences of primers used for qRT-PCR.
    • Supplementary Figure 1. Effects of IGF1R inhibitor on the expression of Na+-K+-2Cl- cotransporter (NKCC) in skin ionocytes in 6-dpf medaka embryos after acute FW to SW transfer. The expression of NKCC (A and D) and Na+-K+-ATPase (NKA) (B and E) were analyzed in 6-dpf medaka embryos by T4 and NKA antibody immunostaining, respectively, after transferred from FW to SW for 0.5 h containing DMSO (A-C) or 2 μM picropodophyllin (PPP) (D-F). Cell nuclei were labeled by DAPI, and the images were merged with NKCC and NKA signals (C and F).
    • Supplementary Figure 2. Changes in Na+-K+-2Cl- cotransporter (NKCC) expression in skin ionocytes in 6-dpf medaka embryos after transfer from FW to SW. Whole embryonic view of the expression of NKCC (A, D, and, G) and Na+-K+-ATPase (NKA) (B, E, and H) in 6-d FW acclimated embryos (A-C), acute FW-SW transfer (D-F), and 6-d SW acclimated embryos (G-I) were analyzed by immunostaining of T4 and NKA antibody. The signals of NKCC in NKAlabeled ionocytes were merely detected in FW acclimated and acute FW-SW transferred embryos, but strongly expressed in SW acclimated embryos. The merge images of NKCC and NKA signals were showed (C, F, and I). The acquisition setting for images is the same for different treatment embryos.
    • Supplementary Figure 3. Changes in the expression of related genes in medaka embryos and adult gills after acclimation to SW. Embryos and adult medaka were acclimated to SW for 6-d and 7-d, respectively. The gene expression was measured by qPCR for igf, igf1ra, igf1rb, nkcc1a, cftr, and NKA alpha subunit isoforms (atp1a1b, atp1a2, atp1a3, and atp1a3b) in 6-dpf embryos (A) and igf, igf1ra, igf1rb, nkcc1a, and cftr in adult gills (B). Values are mean &#x00B1; SD, and sample size is shown in the parentheses. **p < 0.01, ***p < 0.001, ****p < 0.0001 (twotailed unpaired Student&#x2019;s t-test).
    • Supplementary Figure 4. Changes of igfr1b expression in skin ionocytes in 6-dpf medaka embryos after acute FW to SW. In situ hybridization of igfr1b (A-C) and immunostaining of Na+-K+-ATPase (NKA) (D-F) were performed in 6-d FW acclimated embryos (A, D), acute FWSW transfer (B, E), and 6-d SW acclimated embryos (C and F). Scale bar is 100 &#x03BC;m in (C).

 

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  • Bach LA & Hale LJ 2015 Insulin-like growth factors and kidney disease. American Journal of Kidney Diseases 65 327336. (https://doi.org/10.1053/j.ajkd.2014.05.024)

    • Search Google Scholar
    • Export Citation
  • Bath RN & Eddy FB 1979 Salt and water balance in rainbow trout (Salmo gairdneri) rapidly transferred from fresh water to sea water. Journal of Experimental Biology 83 193202.

    • Search Google Scholar
    • Export Citation
  • Blazer-Yost BL & Cox M 1988 Insulin-like growth factor 1 stimulates renal epithelial Na+ transport. American Journal of Physiology 255 C413C417. (https://doi.org/10.1152/ajpcell.1988.255.3.C413)

    • Search Google Scholar
    • Export Citation
  • Blazer-Yost BL, Cox M & Furlanetto R 1989 Insulin and IGF I receptor-mediated Na+ transport in toad urinary bladders. American Journal of Physiology 257 C612C620. (https://doi.org/10.1152/ajpcell.1989.257.4.C612)

    • Search Google Scholar
    • Export Citation
  • Bohnsack BL, Gallina D & Kahana A 2011 Phenothiourea sensitizes zebrafish cranial neural crest and extraocular muscle development to changes in retinoic acid and IGF signaling. PLoS ONE 6 e22991. (https://doi.org/10.1371/journal.pone.0022991)

    • Search Google Scholar
    • Export Citation
  • Bollinger RJ, Madsen SS, Bossus MC & Tipsmark CK 2016 Does Japanese medaka (Oryzias latipes) exhibit a gill Na+/K+-ATPase isoform switch during salinity change? Journal of Comparative Physiology: Part B 186 485501. (https://doi.org/10.1007/s00360-016-0972-6)

    • Search Google Scholar
    • Export Citation
  • Carboni JM, Wittman M, Yang Z, Lee F, Greer A, Hurlburt W, Hillerman S, Cao C, Cantor GH, Dell-John J, 2009 BMS-754807, a small molecule inhibitor of insulin-like growth factor-1R/IR. Molecular Cancer Therapeutics 8 33413349. (https://doi.org/10.1158/1535-7163.MCT-09-0499)

    • Search Google Scholar
    • Export Citation
  • Cozzi RRF, Robertson GN, Spieker M, Claus LN, Zaparilla GMM, Garrow KL & Marshall WS 2015 Paracellular pathway remodeling enhances sodium secretion by teleost fish in hypersaline environments. Journal of Experimental Biology 218 12591269. (https://doi.org/10.1242/jeb.117317)

    • Search Google Scholar
    • Export Citation
  • Dai W, Bai Y, Hebda L, Zhong X, Liu J, Kao J & Duan C 2014 Calcium deficiency-induced and TRP channel-regulated IGF1R-PI3K-Akt signaling regulates abnormal epithelial cell proliferation. Cell Death and Differentiation 21 568581. (https://doi.org/10.1038/cdd.2013.177)

    • Search Google Scholar
    • Export Citation
  • Evans DH, Piermarini PM & Choe KP 2005 The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiological Reviews 85 97177. (https://doi.org/10.1152/physrev.00050.2003)

    • Search Google Scholar
    • Export Citation
  • Flemmer AW, Monette MY, Djurisic M, Dowd B, Darman R, Gimenez I & Forbush B 2010 Phosphorylation state of the Na+-K+-Cl cotransporter (NKCC1) in the gills of Atlantic killifish (Fundulus heteroclitus) during acclimation to water of varying salinity. Journal of Experimental Biology 213 15581566. (https://doi.org/10.1242/jeb.039644)

    • Search Google Scholar
    • Export Citation
  • Foskett JK, Logsdon CD, Turner T, Machen TE & Bern HA 1981 Differentiation of the chloride extrusion mechanism during seawater adaptation of a teleost fish, the cichlid (Sarotherodon mossambicus). Journal of Experimental Biology 93 209224.

    • Search Google Scholar
    • Export Citation
  • Gonzalez-Rodriguez E, Gaeggeler HP & Rossier BC 2007 IGF-1 vs insulin: respective roles in modulating sodium transport via the PI-3 kinase/Sgk1 pathway in a cortical collecting duct cell line. Kidney International 71 116125. (https://doi.org/10.1038/sj.ki.5002018)

    • Search Google Scholar
    • Export Citation
  • Guh YJ & Hwang PP 2017 Insights into molecular and cellular mechanisms of hormonal actions on fish ion regulation derived from the zebrafish model. General and Comparative Endocrinology 251 240240. (https://doi.org/10.1016/j.ygcen.2016.08.009)

    • Search Google Scholar
    • Export Citation
  • Guh YJ, Tseng YC, Yang CY & Hwang PP 2014 Endothelin-1 regulates H+-ATPase-dependent transepithelial H+ secretion in zebrafish. Endocrinology 155 17281737. (https://doi.org/10.1210/en.2013-1775)

    • Search Google Scholar
    • Export Citation
  • Hsu HH, Lin LY, Tseng YC, Horng JL & Hwang PP 2014 A new model for fish ion regulation: identification of ionocytes in freshwater- and seawater-acclimated medaka (Oryzias latipes). Cell and Tissue Research 357 225243. (https://doi.org/10.1007/s00441-014-1883-z)

    • Search Google Scholar
    • Export Citation
  • Hwang PP 1987 Tolerance and ultrastructural responses of branchial chloride cells to salinity changes in the euryhaline teleost Oreochromis mossambicus. Marine Biology 94 643649. (https://doi.org/10.1007/BF00431411)

    • Search Google Scholar
    • Export Citation
  • Hwang PP & Hirano R 1985 Effects of environmental salinity on intercellular organization and junctional structure of chloride cells in early stages of teleost development. Journal of Experimental Zoology 236 115126. (https://doi.org/10.1002/jez.1402360202)

    • Search Google Scholar
    • Export Citation
  • Hwang PP, Lee TH & Lin LY 2011 Ion regulation in fish gills: recent progress in the cellular and molecular mechanisms. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 301 R28R47. (https://doi.org/10.1152/ajpregu.00047.2011)

    • Search Google Scholar
    • Export Citation
  • Hwang PP & Lin LY 2013 Gill ion transport, acid-base regulation and nitrogen excretion. In The Physiology of Fishes, 4th ed., pp 205233. Eds Evans D, Claiborne JB & Currie. S Boca Raton, FL, USA: CRC Press Press.

    • Search Google Scholar
    • Export Citation
  • Hwang PP, Sun CM & Wu SM 1989 Changes of plasma osmolality, chloride concentration and gill Na+-K+-ATPase activity in tilapia Oreochromis mossambicus during seawater acclimation. Marine Biology 100 295299. (https://doi.org/10.1007/BF00391142)

    • Search Google Scholar
    • Export Citation
  • Ilatovskaya DV, Levchenko V, Brands MW, Pavlov TS & Staruschenko A 2015 Cross-talk between insulin and IGF-1 receptors in the cortical collecting duct principal cells: implication for ENaC-mediated Na+ reabsorption. American Journal of Physiology: Renal Physiology 308 F713F719. (https://doi.org/10.1152/ajprenal.00081.2014)

    • Search Google Scholar
    • Export Citation
  • Kamenicky P, Mazziotti G, Lombes M, Giustina A & Chanson P 2014 Growth hormone, insulin-like growth factor-1, and the kidney: pathophysiological and clinical implications. Endocrine Reviews 35 234281. (https://doi.org/10.1210/er.2013-1071)

    • Search Google Scholar
    • Export Citation
  • Ko JA, Murata S & Nishida T 2009 Up-regulation of the tight-junction protein ZO-1 by substance P and IGF-1 in A431 cells. Cell Biochemistry and Function 27 388394. (https://doi.org/10.1002/cbf.1587)

    • Search Google Scholar
    • Export Citation
  • Lara-Diaz VJ, Castilla-Cortazar I, Martin-Estal I, Garcia-Magarino M, Aguirre GA, Puche JE, de la Garza RG, Morales LA & Munoz U 2017 IGF-1 modulates gene expression of proteins involved in inflammation, cytoskeleton, and liver architecture. Journal of Physiology and Biochemistry 73 245258. (https://doi.org/10.1007/s13105-016-0545-x)

    • Search Google Scholar
    • Export Citation
  • Liu C, Xin Y, Bai Y, Lewin G, He G, Mai K & Duan C 2018 Ca2+ concentration-dependent premature death of igfbp5a(−/−) fish reveals a critical role of IGF signaling in adaptive epithelial growth. Science Signaling 11 eaat2231. (https://doi.org/10.1126/scisignal.aat2231)

    • Search Google Scholar
    • Export Citation
  • Lu J, Liu KC, Schulz N, Karampelias C, Charbord J, Hilding A, Rautio L, Bertolino P, Ostenson CG, Brismar K, 2016 IGFBP1 increases beta-cell regeneration by promoting alpha- to beta-cell transdifferentiation. EMBO Journal 35 20262044. (https://doi.org/10.15252/embj.201592903)

    • Search Google Scholar
    • Export Citation
  • Lv J, Zhang D, Liu P & Li J 2016 Effects of salinity acclimation and eyestalk ablation on Na+, K+, 2Cl cotransporter gene expression in the gill of Portunus trituberculatus: a molecular correlate for salt-tolerant trait. Cell Stress & Chaperones 21 829836. (https://doi.org/10.1007/s12192-016-0707-3)

    • Search Google Scholar
    • Export Citation
  • Madsen SS 1990 The role of cortisol and growth hormone in seawater adaptation and development of hypoosmoregulatory mechanisms in sea trout parr (Salmo trutta trutta). General and Comparative Endocrinology 79 111. (https://doi.org/10.1016/0016-6480(90)90082-w)

    • Search Google Scholar
    • Export Citation
  • Madsen SS & Bern HA 1993 In-vitro effects of insulin-like growth factor-I on gill Na+-K+-ATPase in coho salmon, Oncorhynchus kisutch. Journal of Endocrinology 138 2330. (https://doi.org/10.1677/joe.0.1380023)

    • Search Google Scholar
    • Export Citation
  • Marshall WS, Lynch EM & Cozzi RR 2002 Redistribution of immunofluorescence of CFTR anion channel and NKCC cotransporter in chloride cells during adaptation of the killifish Fundulus heteroclitus to sea water. Journal of Experimental Biology 205 12651273.

    • Search Google Scholar
    • Export Citation
  • McCormick SD 1996 Effects of growth hormone and insulin-like growth factor I on salinity tolerance and gill Na+-K+-ATPase in Atlantic salmon (Salmo salar): interaction with cortisol. General and Comparative Endocrinology 101 311. (https://doi.org/10.1006/gcen.1996.0002)

    • Search Google Scholar
    • Export Citation
  • McCormick SD 2001 Endocrine control of osmoregulation in teleost fish. American Zoologist 41 781794.

  • McCormick SD & Bradshaw D 2006 Hormonal control of salt and water balance in vertebrates. General and Comparative Endocrinology 147 38. (https://doi.org/10.1016/j.ygcen.2005.12.009)

    • Search Google Scholar
    • Export Citation
  • Mitsui R, Fujita-Yoshigaki J, Narita T, Matsuki-Fukushima M, Satoh K, Qi B, Guo MY, Katsumata-Kato O & Sugiya H 2010 Maintenance of paracellular barrier function by insulin-like growth factor-I in submandibular gland cells. Archives of Oral Biology 55 963969. (https://doi.org/10.1016/j.archoralbio.2010.07.023)

    • Search Google Scholar
    • Export Citation
  • Moorman BP, Lerner DT, Grau EG & Seale AP 2015 The effects of acute salinity challenges on osmoregulation in Mozambique tilapia reared in a tidally changing salinity. Journal of Experimental Biology 218 731739. (https://doi.org/10.1242/jeb.112664)

    • Search Google Scholar
    • Export Citation
  • Paye JMD, Akers RM, Huckle WR & Forsten-Williams K 2007 Autocrine production of insulin-like growth factor-I (IGF-I) affects paracellular transport across epithelial cells in vitro. Cell Communication and Adhesion 14 8598. (https://doi.org/10.1080/15419060701463116)

    • Search Google Scholar
    • Export Citation
  • Pelis RM & McCormick SD 2001 Effects of growth hormone and cortisol on Na+-K+-2Cl cotransporter localization and abundance in the gills of Atlantic salmon. General and Comparative Endocrinology 124 134143. (https://doi.org/10.1006/gcen.2001.7703)

    • Search Google Scholar
    • Export Citation
  • Prunet P, Pisam M, Claireaux JP, Boeuf G & Rambourg A 1994 Effects of growth hormone on gill chloride cells in juvenile Atlantic salmon (Salmo salar). American Journal of Physiology 266 R850R857. (https://doi.org/10.1152/ajpregu.1994.266.3.R850)

    • Search Google Scholar
    • Export Citation
  • Robertson JD 1957 The habitat of the early vertebrates. Biological Reviews 32 156187. (https://doi.org/10.1111/j.1469-185X.1957.tb01561.x)

    • Search Google Scholar
    • Export Citation
  • Shaw JR, Sato JD, VanderHeide J, LaCasse T, Stanton CR, Lankowski A, Stanton SE, Chapline C, Coutermarsh B, Barnaby R, 2008 The role of SGK and CFTR in acute adaptation to seawater in Fundulus heteroclitus. Cellular Physiology and Biochemistry 22 6978. (https://doi.org/10.1159/000149784)

    • Search Google Scholar
    • Export Citation
  • Shen WP, Horng JL & Lin LY 2011 Functional plasticity of mitochondrion-rich cells in the skin of euryhaline medaka larvae (Oryzias latipes) subjected to salinity changes. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 300 R858R868. (https://doi.org/10.1152/ajpregu.00705.2010)

    • Search Google Scholar
    • Export Citation
  • Staruschenko A, Pochynyuk O, Vandewalle A, Bugaj V & Stockand JD 2007 Acute regulation of the epithelial Na+ channel by phosphatidylinositide 3-OH kinase signaling in native collecting duct principal cells. Journal of the American Society of Nephrology 18 16521661. (https://doi.org/10.1681/ASN.2007010020)

    • Search Google Scholar
    • Export Citation
  • Takei Y, Hiroi J, Takahashi H & Sakamoto T 2014 Diverse mechanisms for body fluid regulation in teleost fishes. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 307 R778R792. (https://doi.org/10.1152/ajpregu.00104.2014)

    • Search Google Scholar
    • Export Citation
  • Takei Y & Hwang PP 2016 Homeostatic responses to osmotic stress. In Fish Physiology – Biology of Stress in Fish. Eds Schreck B, Tort CL, Farrell AP & Brauber CJ Cambridge, MA, USA: Academic Press.

    • Search Google Scholar
    • Export Citation
  • Tipsmark CK & Madsen SS 2009 Distinct hormonal regulation of Na+-K+-atpase genes in the gill of Atlantic salmon (Salmo salar L.). Journal of Endocrinology 203 301310. (https://doi.org/10.1677/JOE-09-0281)

    • Search Google Scholar
    • Export Citation
  • Tsai JC & Hwang PP 1998 Effects of wheat germ agglutinin and colchicine on microtubules of the mitochondria-rich cells and Ca2 + uptake in tilapia (Oreochromis mossambicus) larvae. Journal of Experimental Biology 201 22632271.

    • Search Google Scholar
    • Export Citation
  • Tutau F, Rodriguez-Ortigosa C, Puche JE, Juanarena N, Monreal I, Garcia Fernandez M, Clavijo E, Castilla A & Castilla-Cortazar I 2009 Enhanced actions of insulin-like growth factor-I and interferon-alpha co-administration in experimental cirrhosis. Liver International 29 3746. (https://doi.org/10.1111/j.1478-3231.2008.01770.x)

    • Search Google Scholar
    • Export Citation
  • Waraky A, Akopyan K, Parrow V, Stromberg T, Axelson M, Abrahmsen L, Lindqvist A, Larsson O & Aleem E 2014 Picropodophyllin causes mitotic arrest and catastrophe by depolymerizing microtubules via insulin-like growth factor-1 receptor-independent mechanism. Oncotarget 5 83798392. (https://doi.org/10.18632/oncotarget.2292)

    • Search Google Scholar
    • Export Citation
  • Wong MKS, Tsukada T, Ogawa N, Pipil S, Ozaki H, Suzuki Y, Iwasaki W & Takei Y 2017 A sodium binding system alleviates acute salt stress during seawater acclimation in eels. Zoological Letters 3 22. (https://doi.org/10.1186/s40851-017-0081-8)

    • Search Google Scholar
    • Export Citation
  • Yang WK, Wu YC, Tang CH & Lee TH 2016 Microtubule-dependent changes in morphology and localization of chloride transport proteins in gill mitochondria-rich cells of the tilapia, Oreochromis mossambicus. Journal of Morphology 277 11131122. (https://doi.org/10.1002/jmor.20561)

    • Search Google Scholar
    • Export Citation
  • Zaika O, Palygin O, Tomilin V, Mamenko M, Staruschenko A & Pochynyuk O 2016a Insulin and IGF-1 activate Kir4.1/5.1 channels in cortical collecting duct principal cells to control basolateral membrane voltage. American Journal of Physiology. Renal Physiology 310 F311F321. (https://doi.org/10.1152/ajprenal.00436.2015)

    • Search Google Scholar
    • Export Citation
  • Zaika O, Tomilin V, Mamenko M, Bhalla V & Pochynyuk O 2016b New perspective of ClC-Kb/2 Cl- channel physiology in the distal renal tubule. American Journal of Physiology: Renal Physiology 310 F923F930. (https://doi.org/10.1152/ajprenal.00577.2015)

    • Search Google Scholar
    • Export Citation
  • Zhang Z & Hu J 2007 Development and validation of endogenous reference genes for expression profiling of medaka (Oryzias latipes) exposed to endocrine disrupting chemicals by quantitative real-time RT-PCR. Toxicological Sciences 95 356368. (https://doi.org/10.1093/toxsci/kfl161)

    • Search Google Scholar
    • Export Citation