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Cell proliferation and regeneration in the gill

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Abstract

Seminal studies from the early 20th century defined the structural changes associated with development and regeneration of the gills in goldfish at the gross morphological and cellular levels using standard techniques of light and electron microscopy. More recently, investigations using cell lineage tracing, molecular biology, immunohistochemistry and single-cell RNA-sequencing have pushed the field forward and have begun to reveal the cellular and molecular processes that orchestrate cell proliferation and regeneration in the gills. The gill is a multifunctional organ that mediates an array of important physiological functions, including respiration, ion regulation and excretion of waste products. It is comprised of unique cell types, such as pavement cells, ionocytes, chemoreceptors and undifferentiated stem or progenitor cells that regulate growth and replenish cell populations. The gills develop from the embryonic endoderm and are rich in cell types derived from the neural crest. The gills have the capacity to remodel themselves in response to environmental change, such as in the case of ionocytes, chemoreceptors and the interlamellar cell mass, and can completely regenerate gill filaments and lamellae. Both processes of remodeling and regeneration invariably involve cell proliferation. Although gill regeneration has been reported in only a limited number of fish species, the process appears to have many similarities to regeneration of other organs in fish and amphibians. The present article reviews the studies that have described gill development and growth, and that demonstrate a suite of genes, transcription factors and other proteins involved in cell proliferation and regeneration in the gills.

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Fig. 1

Modified from Stolper et al. (2019) with permission

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Notes

  1. It is important to note that gill neuroepithelial cells (NECs), which are respiratory chemoreceptors, are distinct from neuroepithelial cells of the same name that are important in development of the vertebrate nervous system.

References

  • Alibardi L (2019) Organ regeneration evolved in fish and amphibians in relation to metamorphosis: speculations on a post-embryonic developmental process lost in amniotes after the water to land transition. Ann Anat 222:114–119

    Article  PubMed  Google Scholar 

  • Bailly Y, Dunel-Erb S, Laurent P (1992) The neuroepithelial cells of the fish gill filament: indolamine-immunocytochemistry and innervation. Anat Rec 233:143–161

    Article  CAS  PubMed  Google Scholar 

  • Burkhardt-Holm P, Oulmi Y, Schroeder A, Storch V, Braunbeck T (1999) Toxicity of 4-chloroaniline in early life stages of zebrafish (Danio rerio): II. Cytopathology and regeneration of liver and gills after prolonged exposure to waterborne 4-chloroani- line. Arch Environ Contam Toxicol 37:85–102

    Article  CAS  PubMed  Google Scholar 

  • Burleson ML, Carlton AL, Silva PE (2002) Cardioventilatory effects of acclimatization to aquatic hypoxia in channel catfish. Resp Physiol Neurohiol 131:223–232

    Article  Google Scholar 

  • Burleson ML, Mercer SE, Wilk-Blaszczak MA (2006) Isolation and characterization of putative O2 chemoreceptor cells from the gills of channel catfish (Ictalurus punctatus). Brain Res 1092:100–107

    Article  CAS  PubMed  Google Scholar 

  • Cadiz L, Jonz MG (2020) A comparative perspective on lung and gill regeneration. J Exp Biol 223:jeb226076

    Article  PubMed  Google Scholar 

  • Cadiz L, Reed M, Monis S, Akimenko MA, Jonz MG (2024) Identification of signalling pathways involved in gill regeneration in zebrafish. J Exp Biol 227(2):jeb246290

    Article  PubMed  PubMed Central  Google Scholar 

  • Chang WJ, Horng JL, Yan JJ, Hsiao CD, Hwang PP (2009) The transcription factor, glial cell missing 2, is involved in differentiation and functional regulation of H+-ATPase-rich cells in zebrafish (Danio rerio). Am J Physiol Regul Integr Comp Physiol 296:R1192–1201

    Article  CAS  PubMed  Google Scholar 

  • Chen YC, Liao BK, Lu YF, Liu YH, Hsieh FC, Hwang PP, Hwang SL (2019) Zebrafish Klf4 maintains the ionocyte progenitor population by regulating epidermal stem cell proliferation and lateral inhibition. PLoS Genet 15(4):e1008058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crawford K, Vincenti DM (1998) Retinoic acid and thyroid hormone may function through similar and competitive pathways in regenerating axolotls. J Exp Zool 282:724–738

    Article  CAS  PubMed  Google Scholar 

  • Crump JG, Maves L, Lawson ND, Weinstein BM, Kimmel CB (2004) An essential role for Fgfs in endodermal pouch formation influences later craniofacial skeletal patterning. Development 131:5703–5716

    Article  CAS  PubMed  Google Scholar 

  • Dean BW, Rashid TJ, Jonz MG (2017) Mitogenic action of hypoxia upon cutaneous neuroepithelial cells in developing zebrafish. Dev Neurobiol 77:789–801

    Article  CAS  PubMed  Google Scholar 

  • DeLaurier A (2019) Evolution and development of the fish jaw skeleton. Wiley Interdiscip Rev Dev Biol 8(2):e337

    Article  PubMed  Google Scholar 

  • Dutta HM, Munshi JS, Roy PK, Singh NK, Adhikari S, Killius J (1996) Ultrastructural changes in the respiratory lamellae of the catfish, Heteropneustes fossilis after sublethal exposure to malathion. Environ Pollut 92:329–341

    Article  CAS  PubMed  Google Scholar 

  • Dymowska AK, Hwang PP, Goss GG (2012) Structure and function of ionocytes in the freshwater fish gill. Respir Physiol Neurobiol 184:282–292

    Article  CAS  PubMed  Google Scholar 

  • Esaki M, Hoshijima K, Kobayashi S, Fukuda H, Kawakami K, Hirose S (2007) Visualization in zebrafish larvae of Na+ uptake in mitochondria-rich cells whose differentiation is dependent on foxi3a. Am J Physiol Regul Integr Comp Physiol 292:R470–R480

    Article  CAS  PubMed  Google Scholar 

  • Esaki M, Hoshijima K, Nakamura N, Munakata K, Tanaka M, Ookata K, Asakawa K, Kawakami K, Wang W, Weinberg ES, Hirose S (2009) Mechanism of development of ionocytes rich in vacuolar-type H+-ATPase in the skin of zebrafish larvae. Dev Biol 329:116–129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. Physiol Rev 85:97–177

    Article  CAS  PubMed  Google Scholar 

  • Fabian P, Tseng KC, Thiruppathy M, Arata C, Chen HJ, Smeeton J, Nelson N, Crump JG (2022) Lifelong single-cell profiling of cranial neural crest diversification in zebrafish. Nat Commun 13(1):13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gahlenbeck H, Bartels H (1970) Blood gas transport properties in gill and lung forms of the axolotl (Ambystoma mexicanum). Respir Physiol 9:175–182

    Article  CAS  PubMed  Google Scholar 

  • Gebuijs IGE, Raterman ST, Metz JR, Swanenberg L, Zethof J, Van den Bos R, Carels CEL, Wagener FADTG, Von den Hoff JW (2019) Fgf8a mutation affects craniofacial development and skeletal gene expression in zebrafish larvae. Biol Open 8(9):bio039834

    Article  PubMed  PubMed Central  Google Scholar 

  • Gemberling M, Bailey TJ, Hyde DR, Poss KD (2013) The zebrafish as a model for complex tissue regeneration. Trends Genet 29:611–620

    Article  CAS  PubMed  Google Scholar 

  • Ghanizadeh-Kazerouni E, Wilson JM, Jones SRM, Brauner CJ (2024) Characteristics of a gill resection – regeneration model in freshwater laboratory-reared Atlantic salmon (Salmo salar). Aquaculture 579:740210

    Article  CAS  Google Scholar 

  • Gilbert SF (1988) Developmental Biology, 2nd edn. Sinauer, Sunderland

    Google Scholar 

  • Gillis JA, Tidswell ORA (2017) The origin of vertebrate gills. Curr Biol 27:729–732

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gillis JA, Dahn RD, Shubin NH (2009) Shared developmental mechanisms pattern the vertebrate gill arch and paired fin skeletons. Proc Natl Acad Sci USA 106:5720–5724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goette A (1901) Über die Kiemen Der Fische. Z Wiss Zool 69:533–577

    Google Scholar 

  • Greco AM, Fenwick JC, Perry SF (1996) The effects of soft-water acclimation on gill structure in the rainbow trout Oncorhynchus mykiss. Cell Tissue Res 285:75–82

    Article  CAS  PubMed  Google Scholar 

  • Grotek B, Wehner D, Weidinger G (2013) Notch signaling coordinates cellular proliferation with differentiation during zebrafish fin regeneration. Development 140:1412–1423

    Article  CAS  PubMed  Google Scholar 

  • Hall BK (2009) The neural crest and neural crest cells in Vertebrate Development and Evolution. Springer, New York

    Book  Google Scholar 

  • Hanaoka R, Ohmori Y, Uyemura K, Hosoya T, Hotta Y, Shirao T, Okamoto H (2004) Zebrafish gcmb is required for pharyngeal cartilage formation. Mech Dev 121:1235–1247

    Article  CAS  PubMed  Google Scholar 

  • Hemalatha S, Banerjee TK (1997) Histopathological analysis of sublethal toxicity of zinc chloride to the respiratory organs of the airbreathing catfish Heteropneustes fossilis (Bloch). Biol Res 30:11–21

    CAS  PubMed  Google Scholar 

  • Hockman D, Burns AJ, Schlosser G, Gates KP, Jevans B, Mongera A, Fisher S, Unlu G, Knapik EW, Kaufman CK, Mosimann C, Zon LI, Lancman JJ, Dong PDS, Lickert H, Tucker AS, Baker CV (2017) Evolution of the hypoxia-sensitive cells involved in amniote respiratory reflexes. Elife 6:e21231

    Article  PubMed  PubMed Central  Google Scholar 

  • Hodson EJ, Nicholls LG, Turner PJ, Llyr R, Fielding JW, Douglas G, Ratnayaka I, Robbins PA, Pugh CW, Buckler KJ, Ratcliffe PJ, Bishop T (2016) Regulation of ventilatory sensitivity and carotid body proliferation in hypoxia by the PHD2/HIF-2 pathway. J Physiol 594:1179–1195

    Article  CAS  PubMed  Google Scholar 

  • Hogan BM, Hunter MP, Oates AC, Crowhurst MO, Hall NE, Heath JK, Prince VE, Lieschke GJ (2004) Zebrafish gcm2 is required for gill filament budding from pharyngeal ectoderm. Dev Biol 276:508–522

    Article  CAS  PubMed  Google Scholar 

  • Hsiao C, You M, Guh Y, Ma M, Jiang Y, Hwang P (2007) A positive regulatory loop between foxi3a and foxi3b is essential for specification and differentiation of zebrafish epidermal ionocytes. PLoS ONE 2:e302

  • Hughes GM (1984) General anatomy of the gills. In: Hoar WS, Randall DJ (eds) Fish physiology, vol XA. Academic, San Diego, pp 1–72

    Google Scholar 

  • Jackson R, Braubach OR, Bilkey J, Zhang J, Akimenko MA, Fine A, Croll RP, Jonz MG (2013) Expression of sall4 in taste buds of zebrafish. Dev Neurobiol 73:543–558

    Article  CAS  PubMed  Google Scholar 

  • Janicke M, Carney TJ, Hammerschmidt M (2007) Foxi3 transcription factors and notch signaling control the formation of skin ionocytes from epidermal precursors of the zebrafish embryo. Dev Biol 307:258–271

    Article  PubMed  Google Scholar 

  • Jonz MG, Nurse CA (2003) Neuroepithelial cells and associated innervation of the zebrafish gill: a confocal immunofluorescence study. J Comp Neurol 461:1–17

    Article  PubMed  Google Scholar 

  • Jonz MG, Nurse CA (2005) Development of oxygen sensing in the gills of zebrafish. J Exp Biol 208:1537–1549

    Article  PubMed  Google Scholar 

  • Jonz MG, Fearon IM, Nurse CA (2004) Neuroepithelial oxygen chemoreceptors of the zebrafish gill. J Physiol 560:737–752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jonz MG, Zachar PC, Da Fonte DF, Mierzwa AS (2015) Peripheral chemoreceptors in fish: a brief history and a look ahead. Comp Biochem Physiol Mol Integr Physiol 186:27–38

    Article  CAS  Google Scholar 

  • Kameda Y (2005) Mash1 is required for glomus cell formation in the mouse carotid body. Dev Biol 283:128–139

    Article  CAS  PubMed  Google Scholar 

  • Kapsimali M, Kaushik A-L, Gibon G, Dirian L, Ernest S, Rosa FM (2011) Fgf signaling controls pharyngeal taste bud formation through miR-200 and Delta-Notch activity. Development 138:3473–3484

    Article  PubMed  Google Scholar 

  • Katoh F, Kaneko T (2003) Short-term transformation and long-term replacement of branchial chloride cells in killifish transferred from seawater to freshwater, revealed by morphofunctional observations and a newly established ‘time-differential double fluorescent staining’ technique. J Exp Biol 206:4113–4123

    Article  PubMed  Google Scholar 

  • Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253–310

    Article  CAS  PubMed  Google Scholar 

  • Kumai Y, Kwong RW, Perry SF (2015) A role for transcription factor glial cell missing 2 in Ca2+ homeostasis in zebrafish, Danio rerio. Pflügers Arch 467:753–765

    Article  CAS  PubMed  Google Scholar 

  • Kwong RW, Perry SF (2015) An essential role for parathyroid hormone in gill formation and differentiation of ion-transporting cells in developing zebrafish. Endocrinology 156:2384–2394

    Article  CAS  PubMed  Google Scholar 

  • Landacre FL (1921) The fate of the NC in the head of the Urodeles. J Comp Neurol 33:1–43

    Article  Google Scholar 

  • Laurent P (1984) Gill internal morphology. In: Hoar WS, Randall DJ (eds) Fish physiology, vol XA. Academic, San Diego, pp 73–183

    Google Scholar 

  • Laurent P, Dunel S (1980) Morphology of gill epithelia in fish. Am J Physiol 238:R147–159

    CAS  PubMed  Google Scholar 

  • Lazcano I, Olvera A, Pech-Pool SM, Sachs L, Buisine N, Orozco A (2023) Differential effects of 3,5-T2 and T3 on the gill regeneration and metamorphosis of the Ambystoma mexicanum (axolotl). Front Endocrinol 14:1208182

    Article  CAS  Google Scholar 

  • Le Lièvre CS, Le Douarin NM (1975) Mesenchymal derivatives of the neural crest: analysis of chimaeric quail and chick embryos. J Embryol Exp Morphol 34:125–154

    PubMed  Google Scholar 

  • Logan CY, Nusse R (2004) The wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20:781–810

    Article  CAS  PubMed  Google Scholar 

  • Mandic M, Joyce W, Perry SF (2021) The evolutionary and physiological significance of the Hif pathway in teleost fishes. J Exp Biol 224:jeb231936

    Article  PubMed  Google Scholar 

  • Marcos-López M, Rodger HD (2020) Amoebic gill disease and host response in Atlantic salmon (Salmo salar L.): a review. Parasite Immunol 42:e12766

    Article  PubMed  Google Scholar 

  • McBryan TL, Healy TM, Haakons KL, Schulte PM (2016) Warm acclimation improves hypoxia tolerance in Fundulus heteroclitus. J Exp Biol 219:474–484

    Article  PubMed  Google Scholar 

  • McCormick SD, Regish AM, Christensen AK, Björnsson BT (2013) Differential regulation of sodium-potassium pump isoforms during smolt development and seawater exposure of Atlantic salmon. J Exp Biol 216:1142–1151

    Article  CAS  PubMed  Google Scholar 

  • Mierzwa AS, Nguyen F, Xue M, Jonz MG (2020) Regeneration of the gill filaments and replacement of serotonergic neuroepithelial cells in adult zebrafish (Danio rerio). Respir Physiol Neurobiol 274:103366

    Article  CAS  PubMed  Google Scholar 

  • Mitrovic D, Perry SF (2009) The effects of thermally induced gill remodeling on ionocyte distribution and branchial chloride fluxes in goldfish (Carassius auratus). J Exp Biol 212:843–852

    Article  CAS  PubMed  Google Scholar 

  • Mokhtar DM, Sayed RKA, Zaccone G, Alesci A, Hussein MM (2023) The potential role of the pseudobranch of molly fish (Poecilia sphenops) in immunity and cell regeneration. Sci Rep 13(1):8665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mongera A, Singh AP, Levesque MP, Chen YY, Konstantinidis P, Nüsslein-Volhard C (2013) Genetic lineage labeling in zebrafish uncovers novel neural crest contributions to the head, including gill pillar cells. Development 140:916–925

    Article  CAS  PubMed  Google Scholar 

  • Moreno-Domínguez A, Ortega-Sáenz P, Gao L, Colinas O, García-Flores P, Bonilla-Henao V, Aragonés J, Hüttemann M, Grossman LI, Weissmann N, Sommer N, López-Barneo J (2020) Acute O2 sensing through HIF2α-dependent expression of atypical cytochrome oxidase subunits in arterial chemoreceptors. Sci Signal 13(615):eaay9452

    Article  PubMed  Google Scholar 

  • Morgan M (1974a) The development of gill arches and gill blood vessels of the rainbow trout, Salmo Gairdneri. J Morphol 142:351–363

    Article  PubMed  Google Scholar 

  • Morgan M (1974b) Development of secondary lamellae of the gills of the trout, Salmo Gairdneri (Richardson). Cell Tissue Res 151:509–523

    Article  CAS  PubMed  Google Scholar 

  • Münch J, González-Rajal A, de la Pompa JL (2013) Notch regulates blastema proliferation and prevents differentiation during adult zebrafish fin regeneration. Development 140:1402–1411

    Article  PubMed  Google Scholar 

  • Neff AW, King MW, Mescher AL (2011) Dedifferentiation and the role of sall4 in reprogramming and patterning during amphibian limb regeneration. Dev Dyn 240:979–989

    Article  CAS  PubMed  Google Scholar 

  • Nguyen F, Jonz MG (2021) Replacement of mitochondrion-rich cells during regeneration of the gills and opercular epithelium in zebrafish (Danio rerio). Acta Histochem 123:151738

    Article  CAS  PubMed  Google Scholar 

  • Nilsson S (1984) Innervation and pharmacology of the gills. In: Hoar WS, Randall DJ (eds) Fish physiology, vol XA. Academic, San Diego, pp 185–227

    Google Scholar 

  • Nilsson GE, Dymowska A, Stecyk JA (2012) New insights into the plasticity of gill structure. Respir Physiol Neurobiol 184:214–222

    Article  PubMed  Google Scholar 

  • Nye HLD, Cameron JA, Chernoff EAG, Stocum DL (2003) Regeneration of the urodele limb: a review. Dev Dyn 226:280–294

    Article  PubMed  Google Scholar 

  • Olson KR (2002) Vascular anatomy of the fish gill. J Exp Zool 293:214–231

    Article  PubMed  Google Scholar 

  • Ong KJ, Stevens ED, Wright PA (2007) Gill morphology of the mangrove killifish (Kryptolebias Marmoratus) is plastic and changes in response to terrestrial air exposure. J Exp Biol 210:1109–1115

    Article  CAS  PubMed  Google Scholar 

  • Ortega-Sáenz P, López-Barneo J (2020) Physiology of the carotid body: from molecules to disease. Annu Rev Physiol 82:127–149

    Article  PubMed  Google Scholar 

  • Pan W, Scott AL, Nurse CA, Jonz MG (2021) Identification of oxygen-sensitive neuroepithelial cells through an endogenous reporter gene in larval and adult transgenic zebrafish. Cell Tissue Res 384:35–47

    Article  CAS  PubMed  Google Scholar 

  • Pan W, Godoy RS, Cook DP, Scott AL, Nurse CA, Jonz MG (2022) Single-cell transcriptomic analysis of neuroepithelial cells and other cell types of the gills of zebrafish (Danio rerio) exposed to hypoxia. Sci Rep 12(1):10144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pardal R, Ortega-Sáenz P, Durán R, López-Barneo J (2007) Glia-like stem cells sustain physiologic neurogenesis in the adult mammalian carotid body. Cell 131:364–377

    Article  CAS  PubMed  Google Scholar 

  • Pearse AG, Polak JM, Rost FW, Fontaine J, Le Lièvre C, Le Douarin N (1973) Demonstration of the neural crest origin of type I (APUD) cells in the avian carotid body, using a cytochemical marker system. Histochemie 34:191–203

    Article  CAS  PubMed  Google Scholar 

  • Porteus CS, Abdallah SJ, Pollack J, Kumai Y, Kwong RW, Yew HM, Milsom WK, Perry SF (2014) The role of hydrogen sulphide in the control of breathing in hypoxic zebrafish (Danio rerio). J Physiol 592:3075–3088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poss KD, Shen J, Keating MT (2000) Induction of lef1 during zebrafish fin regeneration. Dev Dyn 219:282–286

    Article  CAS  PubMed  Google Scholar 

  • Poss KD, Keating MT, Nechiporuk A (2003) Tales of regeneration in zebrafish. Dev Dyn 226:202–210

    Article  PubMed  Google Scholar 

  • Qin Z, Lewis JE, Perry SF (2010) Zebrafish (Danio rerio) gill neuroepithelial cells are sensitive chemoreceptors for environmental CO2. J Physiol 588:861–872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosenkilde P, Ussing AP (1996) What mechanisms control neoteny and regulate induced metamorphosis in urodeles? Int J Dev Biol 40:665–673

    CAS  PubMed  Google Scholar 

  • Saito N, Nishimura K, Makanae A, Satoh A (2019) Fgf- and bmp- signaling regulate gill regeneration in Ambystoma mexicanum. Dev Biol 452:104–113

    Article  CAS  PubMed  Google Scholar 

  • Schäfer W (1936) Die Regeneration der Kiemen und Flossenstrahlen beim Goldfisch (Carassius auratus). Jena Z Naturw 70:303–358

  • Semenza GL (2012) Hypoxia-inducible factors in physiology and medicine. Cell 148:399–408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sheehan-Rooney K, Swartz ME, Zhao F, Liu D, Eberhart JK (2013) Ahsa1 and Hsp90 activity confers more severe craniofacial phenotypes in a zebrafish model of hypoparathyroidism, sensorineural deafness and renal dysplasia (HDR). Dis Model Mech 6:1285–1291

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shimizu N, Kawakami K, Ishitani T (2012) Visualization and exploration of Tcf/Lef function using a highly responsive Wnt/β-catenin signaling-reporter transgenic zebrafish. Dev Biol 370:71–85

    Article  CAS  PubMed  Google Scholar 

  • Shono T, Kurokawa D, Miyake T, Okabe M (2011) Acquisition of glial cells missing 2 enhancers contributes to a diversity of ionocytes in zebrafish. PLoS ONE 6(8):e23746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sollid J, De Angelis P, Gundersen K, Nilsson GE (2003) Hypoxia induces adaptive and reversible gross morphological changes in crucian carp gills. J Exp Biol 206:3667–3673

    Article  PubMed  Google Scholar 

  • Sollid J, Weber RE, Nilsson GE (2005) Temperature alters the respiratory surface area of crucian carp Carassius carassius and goldfish Carassius auratus. J Exp Biol 208:1109–1116

    Article  PubMed  Google Scholar 

  • Stocum DL (2017) Mechanisms of urodele limb regeneration. Regeneration 4:159–200

    Article  PubMed  PubMed Central  Google Scholar 

  • Stolper J, Ambrosio EM, Danciu DP, Buono L, Elliott DA, Naruse K, Martínez-Morales JR, Marciniak-Czochra A, Centanin L (2019) Stem cell topography splits growth and homeostatic functions in the fish gill. Elife 8:e43747

    Article  PubMed  PubMed Central  Google Scholar 

  • Sundin L, Nilsson S (2002) Branchial innervation. J Exp Zool 293:232–248

    Article  PubMed  Google Scholar 

  • Tal TL, Franzosa JA, Tanguay RL (2010) Molecular signaling networks that choreograph epimorphic fin regeneration in zebrafish - a mini-review. Gerontology 56:231–240

    Article  CAS  PubMed  Google Scholar 

  • Vulesevic B, McNeill B, Perry SF (2006) Chemoreceptor plasticity and respiratory acclimation in the zebrafish Danio rerio. J Exp Biol 209:1261–1273

    Article  CAS  PubMed  Google Scholar 

  • Warga RM, Nüsslein-Volhard C (1999) Origin and development of the zebrafish endoderm. Development 126:827–838

    Article  CAS  PubMed  Google Scholar 

  • West AC, Mizoro Y, Wood SH, Ince LM, Iversen M, Jørgensen EH, Nome T, Sandve SR, Martin SAM, Loudon ASI, Hazlerigg DG (2021) Immunologic profiling of the Atlantic salmon gill by single nuclei transcriptomics. Front Immunol 12:669889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson JM, Laurent P (2002) Fish Gill morphology: inside out. J Exp Zool 293:192–213

    Article  PubMed  Google Scholar 

  • Xu XN, Chen SL, Jiang ZX, Nissa MU, Zou SM (2002) Gill remodeling increases the respiratory surface area of grass carp (Ctenopharyngodon idella) under hypoxic stress. Comp Biochem Physiol Mol Integr Physiol 272:111278

    Article  Google Scholar 

  • Yang J, Chai L, Fowles TC, Alipio Z, Xu D, Fink LM, Ward DC, Ma Y (2008) Genome-wide analysis reveals Sall4 to be a major regulator of pluripotency in murine-embryonic stem cells. Proc Natl Acad Sci USA 105:19756–19761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Tam WL, Tong GQ, Wu Q, Chan HY, Soh BS, Lou Y, Yang J, Ma Y, Chai L, Ng HH, Lufkin T, Robson P, Lim B (2006) Sall4 modulates embryonic stem cell pluripotency and early embryonic development by the transcriptional regulation of Pou5f1. Nat Cell Biol 8:1114–1123

    Article  CAS  PubMed  Google Scholar 

  • Zheng S, Wang WX (2023) Physiological and immune profiling of tilapia Oreochromis Niloticus gills by high-throughput single-cell transcriptome sequencing. Fish Shellfish Immunol 141:109070

    Article  CAS  PubMed  Google Scholar 

  • Zheng D, Kille P, Feeney GP, Cunningham P, Handy RD, Hogstrand C (2010) Dynamic transcriptomic profiles of zebrafish gills in response to zinc supplementation. BMC Genomics 11:553

    Article  PubMed  PubMed Central  Google Scholar 

  • Zimmer AM, Goss GG, Glover CN (2021) Reductionist approaches to the study of ionoregulation in fishes. Comp Biochem Physiol B Biochem Mol Biol 255:110597

    Article  CAS  PubMed  Google Scholar 

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Research support was provided by a grant from the Natural Sciences and Engineering Research Council of Canada (grant no. 05571).

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  1. Department of Biology, University of Ottawa, 30 Marie Curie Pvt, Ottawa, ON, K1N 6N5, Canada

    Michael G. Jonz

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Jonz, M.G. Cell proliferation and regeneration in the gill. J Comp Physiol B (2024). https://doi.org/10.1007/s00360-024-01548-2

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