Exploring the regulatory role of nitric oxide (NO) and the NO-p38MAPK/cGMP pathway in larval settlement of the bryozoan Bugula neritina

References

• Alfaro AC, Young T, Ganesan AM. 2011. Regulatory effects of mussel (Aulacomya maoriana Iredale 1915) larval settlement by neuroactive compounds, amino acids and bacterial biofilms. Aquaculture. 322-323:158–168. doi: 10.1016/j.aquaculture.2011.08.038.10.1016/j.aquaculture.2011.08.038
   Web of Science ®Google Scholar
• Bhat NR, Zhang P, Lee JC, Hogan EL. 1998. Extracellular signal-regulated kinase and p38 subgroups of mitogen-activated protein kinases regulate inducible nitric oxide synthase and tumor necrosis factor-α gene expression in endotoxin-stimulated primary glial cultures. J Neurosci. 18:1633–1641. doi: 10.1523/JNEUROSCI.18-05-01633.1998.10.1523/JNEUROSCI.18-05-01633.1998
   PubMed Web of Science ®Google Scholar
• Biggers WJ, Pires A, Pechenik JA, Johns E, Patel P, Polson T, Polson J. 2012. Inhibitors of nitric oxide synthase induce larval settlement and metamorphosis of the polychaete annelid Capitella teleta. Invertebr Reprod Dev. 56:1–13. doi: 10.1080/07924259.2011.588006.10.1080/07924259.2011.588006
   Web of Science ®Google Scholar
• Bishop CD, Brandhorst BP. 2001. NO/cGMP signaling and HSP90 activity represses metamorphosis in the sea urchin Lytechinus pictus. Biol Bull. 201:394–404. doi: 10.2307/1543617.10.2307/1543617
   PubMed Web of Science ®Google Scholar
• Bishop CD, Brandhorst BP. 2003. On nitric oxide signaling, metamorphosis, and the evolution of biphasic life cycles. Evol Dev. 5:542–550. doi: 10.1046/j.1525-142X.2003.03059.x.10.1046/j.1525-142X.2003.03059.x
   PubMed Web of Science ®Google Scholar
• Bishop CD, Bates WR, Brandhorst BP. 2001. Regulation of metamorphosis in ascidians involves NO/cGMP signaling and HSP90. J Exp Zool(6). 289:374–384. doi: 10.1002/(ISSN)1097-010X.10.1002/(ISSN)1097-010X
   PubMedGoogle Scholar
• Bishop CD, Pires A, Norby SW, Boudko D, Moroz LL, Hadfield MG. 2008. Analysis of nitric oxide-cyclic guanosine monophosphate signaling during metamorphosis of the nudibranch Phestilla sibogae Bergh (Gastropoda: Opisthobranchia). Evol Dev. 10:288–299. doi: 10.1111/j.1525-142X.2008.00238.x.10.1111/j.1525-142X.2008.00238.x
   PubMed Web of Science ®Google Scholar
• Bloodgood RA. 2010. Sensory reception is an attribute of both primary cilia and motile cilia. J Cell Sci. 123:505–509. doi: 10.1242/jcs.066308.10.1242/jcs.066308
   PubMed Web of Science ®Google Scholar
• Bruckdorfer R. 2005. The basics about nitric oxide. Mol Aspects Med. 26:3–31. doi: 10.1016/j.mam.2004.09.002.10.1016/j.mam.2004.09.002
   PubMedGoogle Scholar
• Brunner F, Stessel H, Kukovetz WR. 1995. Novel guanylyl cyclase inhibitor, ODQ reveals role of nitric oxide, but not of cyclic GMP in endothelin-1 secretion. FEBS Lett. 376:262–266. doi: 10.1016/0014-5793(95)01297-X.10.1016/0014-5793(95)01297-X
   PubMed Web of Science ®Google Scholar
• Bryan PJ, Qian PY. 1998. Induction of larval attachment and metamorphosis in the abalone Haliotis diversicolor (Reeve). J Exp Mar Biol Ecol. 223:39–51. doi: 10.1016/S0022-0981(97)00156-1.10.1016/S0022-0981(97)00156-1
   Web of Science ®Google Scholar
• Carpizo-Ituarte E, Hadfield MG. 1998. Stimulation of metamorphosis in the Polychaete Hydroides elegans Haswell (Serpulidae). Biol Bull. 194:14–24. doi: 10.2307/1542509.10.2307/1542509
   PubMed Web of Science ®Google Scholar
• Comes S, Locascio A, Silvestre F, d’Ischia M, Russo GL, Tosti E, Branno M, Palumbo A. 2007. Regulatory roles of nitric oxide during larval development and metamorphosis in Ciona intestinalis. Developmental Biology. 306:772–784. doi: 10.1016/j.ydbio.2007.04.016.10.1016/j.ydbio.2007.04.016
   PubMed Web of Science ®Google Scholar
• Coulthard LR, White DE, Jones DL, McDermott MF, Burchill SA. 2009. p38 MAPK: stress responses from molecular mechanisms to therapeutics. Trends Mol Med. 15:369–379. doi: 10.1016/j.molmed.2009.06.005.10.1016/j.molmed.2009.06.005
   PubMed Web of Science ®Google Scholar
• Couper JM, Leise EM. 1996. Serotonin injections induce metamorphosis in larvae of the gastropod mollusc Ilyanassa obsoleta. Biol Bull. 191:178–186. doi: 10.2307/1542921.10.2307/1542921
   PubMed Web of Science ®Google Scholar
• Dobretsov SV, Qian PY. 2003. Pharmacological induction of larval settlement and metamorphosis in the blue mussel Mytilus edulis L. Biofouling. 19:57–63. doi: 10.1080/0892701021000060860.10.1080/0892701021000060860
   PubMed Web of Science ®Google Scholar
• Elphick MR, Kemenes G, Staras K, O’Shea M. 1995. Behavioral role for nitric oxide in chemosensory activation of feeding in a mollusc. J Neurosci. 15:7653–7664. doi: 10.1523/JNEUROSCI.15-11-07653.1995.10.1523/JNEUROSCI.15-11-07653.1995
   PubMed Web of Science ®Google Scholar
• Fedele E, Jin Y, Varnier G, Raiteri M. 1996. In vivo microdialysis study of a specific inhibitor of soluble guanylyl cyclase on the glutamate receptor/nitric oxide/cyclic GMP pathway. Br J Pharmacol. 119:590–594. doi: 10.1111/bph.1996.119.issue-3.10.1111/bph.1996.119.issue-3
   PubMed Web of Science ®Google Scholar
• Froggett SJ, Leise EM. 1999. Metamorphosis in the marine snail Ilyanassa obsoleta, Yes or NO? Biol Bull. 196:57–62. doi: 10.2307/1543167.10.2307/1543167
   PubMed Web of Science ®Google Scholar
• Fusetani N. 2004. Biofouling and antifouling. Nat Prod Rep. 21:94–104. doi: 10.1039/b302231p.10.1039/b302231p
   PubMed Web of Science ®Google Scholar
• Grossi L, D’Angelo S. 2005. Sodium Nitroprusside: Mechanism of NO release mediated by sulfhydryl-containing molecules. J Med Chem. 48:2622–2626. doi: 10.1021/jm049857n.10.1021/jm049857n
   PubMed Web of Science ®Google Scholar
• Haase A, Bicker G. 2003. Nitric oxide and cyclic nucleotides are regulators of neuronal migration in an insect embryo. Development. 130:3977–3987. doi: 10.1242/dev.00612.10.1242/dev.00612
   PubMed Web of Science ®Google Scholar
• He LS, Xu Y, Matsumura K, Zhang Y, Zhang G, Qi SHI, Qian PY. 2012. Evidence for the involvement of p38 MAPK activation in barnacle larval settlement. PLoS ONE. 7:e47195. doi: 10.1371/journal.pone.0047195.10.1371/journal.pone.0047195
   PubMed Web of Science ®Google Scholar
• Hensley K, Robinson KA, Gabbita SP, Salsman S, Floyd RA. 2000. Reactive oxygen species, cell signaling, and cell injury. Free Radical Biol Med. 28:1456–1462. doi: 10.1016/S0891-5849(00)00252-5.10.1016/S0891-5849(00)00252-5
   PubMed Web of Science ®Google Scholar
• Huang G, Shi LZ, Chi H. 2009. Regulation of JNK and p38 MAPK in the immune system: signal integration, propagation and termination. Cytokine. 48:161–169.doi: 10.1016/j.cyto.2009.08.002.10.1016/j.cyto.2009.08.002
   PubMed Web of Science ®Google Scholar
• Johnson JL, Leroux MR. 2010. cAMP and cGMP signaling: sensory systems with prokaryotic roots adopted by eukaryotic cilia. Trends Cell Biol. 20:435–444. doi: 10.1016/j.tcb.2010.05.005.10.1016/j.tcb.2010.05.005
   PubMed Web of Science ®Google Scholar
• Kojima H, Nakatsubo N, Kikuchi K, Kawahara S, Kirino Y, Nagoshi H, Hirata Y, Nagano T. 1998. Detection and imaging of nitric oxide with novel fluorescent indicators: diaminofluoresceins. Anal Chem. 70:2446–2453. doi: 10.1021/ac9801723.10.1021/ac9801723
   PubMed Web of Science ®Google Scholar
• Kronstrom J, Dupont S, Mallefet J, Thorndyke M, Holmgren S. 2007. Serotonin and nitric oxide interaction in the control of bioluminescence in northern krill, Meganyctiphanes norvegica (M. Sars). J Exp Biol. 210:3179–3187. doi: 10.1242/jeb.002394.10.1242/jeb.002394
   PubMed Web of Science ®Google Scholar
• Leise EM, Kempf SC, Durham NR, Gifondorwa DJ. 2004. Induction of metamorphosis in the marine gastropod Ilyanassa obsoleta : 5HT, NO and programmed cell death. Acta Biol Hung. 55:293–300. doi: 10.1556/ABiol.55.2004.1-4.35.10.1556/ABiol.55.2004.1-4.35
   PubMed Web of Science ®Google Scholar
• Letunic I, Doerks T, Bork P. 2014. SMART: recent updates, new developments and status in 2015. Nucleic Acids Res. 43:D257–D260.
   PubMed Web of Science ®Google Scholar
• Li H, Wei Lin W, Zhang G, Cai Z, Cai G, Chang Y, Xing K. 2006. Enhancement of larval settlement and metamorphosis through biological and chemical cues in the abalone Haliotis diversicolor supertexta. Aquaculture. 258:416–423. doi: 10.1016/j.aquaculture.2006.04.013.10.1016/j.aquaculture.2006.04.013
   Web of Science ®Google Scholar
• Lucas KA, Pitari GM, Kazerouni S, Ruiz-Stewart I, Park J, Schulz S, Chepenik KP, Waldman SA. 2000. Guanylyl cyclases and signaling by cyclic GMP. Pharmacol Rev. 52:375–414.
   PubMed Web of Science ®Google Scholar
• Marshall DJ, Pechenik JA, Keough MJ. 2003. Larval activity levels and delayed metamorphosis affect post-larval performance in the colonial ascidian Diplosoma listerianum. Mar Ecol Prog Ser. 246:153–162. doi: 10.3354/meps246153.10.3354/meps246153
   Web of Science ®Google Scholar
• Moncada S, Palmer RM, Higgs EA. 1991. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev. 43:109–142.
   PubMed Web of Science ®Google Scholar
• Palumbo A. 2005. Nitric oxide in marine invertebrates: a comparative perspective. Comp Biochem Physiol A: Mol Integr Physiol. 142:241–248. doi: 10.1016/j.cbpb.2005.05.043.10.1016/j.cbpb.2005.05.043
   PubMed Web of Science ®Google Scholar
• Pearce CM, Scheibling RE. 1994. Induction of metamorphosis of larval echinoids (Strongylocentrotus droebachiensis and Echinarachnius parma) by potassium chloride (KCI). Invertebr Reprod Dev. 26:213–220. doi: 10.1080/07924259.1994.9672420.10.1080/07924259.1994.9672420
   Web of Science ®Google Scholar
• Pechenik JA, Heyman WD. 1987. Using KCl to determine size at competence for larvae of the marine gastropod Crepidula fornicata (L.). J Exp Mar Biol Ecol. 112:27–38. doi: 10.1016/S0022-0981(87)80012-6.10.1016/S0022-0981(87)80012-6
   Web of Science ®Google Scholar
• Pechenik JA, Qian PY. 1998. Onset and maintenance of metamorphic competence in the marine polychaete Hydroides elegans Haswell in response to three chemical cues. J Exp Mar Biol Ecol. 226:51–74. doi: 10.1016/S0022-0981(97)00237-2.10.1016/S0022-0981(97)00237-2
   Web of Science ®Google Scholar
• Pechenik JA, Cochrane DE, Li W, West ET, Pires A, Leppo M. 2007. Nitric oxide inhibits metamorphosis in larvae of Crepidula fornicata, the Slippershell Snail. Biol Bull. 213:160–171. doi: 10.2307/25066632.10.2307/25066632
   PubMed Web of Science ®Google Scholar
• Pfeiffer S, Leopold E, Hemmens B, Schmidt K, Werner ER, Mayer B. 1997. Interference of carboxy-PTIO with nitric oxide- and peroxynitrite-mediated reactions. Free Radic Biol Med. 22:787–794. doi: 10.1016/S0891-5849(96)00407-8.10.1016/S0891-5849(96)00407-8
   PubMed Web of Science ®Google Scholar
• Pires A, Woollacott RM. 1997. Serotonin and dopamine have opposite effects on phototaxis in larvae of the bryozoan Bugula neritina. Biol Bull. 192:399–409. doi: 10.2307/1542749.10.2307/1542749
   PubMed Web of Science ®Google Scholar
• Qian PY. 1999. Larval settlement of polychaetes. Hydrobiologia. 402:239–253. doi: 10.1023/A:1003704928668.10.1023/A:1003704928668
   Web of Science ®Google Scholar
• Reed CG, Woollacott RM. 1982. Mechanisms of rapid morphogenetic movements in the metamorphosis of the bryozoan Bugula neritina (Cheilostomata, Cellularioidea) I Attachment to the substratum. J Morphol. 172:335–348. doi: 10.1002/(ISSN)1097-4687.10.1002/(ISSN)1097-4687
   PubMed Web of Science ®Google Scholar
• Reed CG, Woollacott RM. 1983. Mechanisms of rapid morphogenetic movements in the metamorphosis of the bryozoan Bugula neritina (Cheilostomata, Cellularioidea) II The role of dynamic assemblages of microfilaments in the pallial epithelium. J Morphol. 177:127–143. doi: 10.1002/(ISSN)1097-4687.10.1002/(ISSN)1097-4687
   Web of Science ®Google Scholar
• Reed CG, Ninos JM, Woollacott RM. 1988. Bryozoan larvae as mosaics of multifunctional ciliary fields: ultrastructure of the sensory organs of Bugula solonifera (Cheilostomata: Cellularioidea). J Morphol. 197:127–145. doi: 10.1002/(ISSN)1097-4687.10.1002/(ISSN)1097-4687
   PubMed Web of Science ®Google Scholar
• Rodriguez SRRS, Ojeda FP, Inestrosa NG. 1993. Settlement of benthic marine invertebrates. Mar Ecol Prog Ser. 97:193–207. doi: 10.3354/meps097193.10.3354/meps097193
   Web of Science ®Google Scholar
• Romero MR, Phuong MA, Bishop C, Krug PJ. 2013. Nitric oxide signaling differentially affects habitat choice by two larval morphs of the sea slug Alderia willowi: mechanistic insight into evolutionary transitions in dispersal strategies. J Exp Biol. 216:1114–1125. doi: 10.1242/jeb.080747.10.1242/jeb.080747
   PubMed Web of Science ®Google Scholar
• Santagata S. 2008a. The morphology and evolutionary significance of the ciliary fields and musculature among marine bryozoan larvae. J Morphol. 269:349–364. doi: 10.1002/(ISSN)1097-4687.10.1002/(ISSN)1097-4687
   PubMed Web of Science ®Google Scholar
• Santagata S. 2008b. Evolutionary and structural diversification of the larval nervous system among marine bryozoans. Biol Bull. 215:3–23.
   PubMed Web of Science ®Google Scholar
• Shimizu K, Hunter E, Fusetani N. 2000. Localisation of biogenic amines in larvae of Bugula neritina (Bryozoa: Cheilostomatida) and their effects on settlement. Mar Biol. 136:1–9. doi: 10.1007/s002270050001.10.1007/s002270050001
   Web of Science ®Google Scholar
• Ueda N, Degnan SM. 2013. Nitric oxide acts as a positive regulator to induce metamorphosis of the ascidian Herdmania momus. PLoS ONE. 8:e72797. doi: 10.1371/journal.pone.0072797.10.1371/journal.pone.0072797
   PubMed Web of Science ®Google Scholar
• Ueda N, Degnan SM. 2014. Nitric oxide is not a negative regulator of metamorphic induction in the abalone Haliotis asinine. Front Mar Sci. 1:1–13.
   Google Scholar
• Ueda N, Richards GS, Degnan BM, Kranz A, Adamska M, Croll RP, Degnan SM. 2016. An ancient role for nitric oxide in regulating the animal pelagobenthic life cycle: evidence from a marine sponge. Sci Rep. 6:437. doi: 10.1038/srep37546.10.1038/srep37546
   Web of Science ®Google Scholar
• Wang H, Qian PY. 2010. Involvement of a novel p38 mitogen-activated protein kinase in larval metamorphosis of the polychaete Hydroides elegans (Haswell). J Exp Zool B. 314B:390–402. doi: 10.1002/jez.b.v314b:5.10.1002/jez.b.v314b:5
   Google Scholar
• Wang H, Zhang H, Wong YH, Voolstra C, Ravasi T, Bajic VladimirB, Qian Pei-YuanV, Qian PY. 2010. Rapid transcriptome and proteome profiling of a non-model marine invertebrate, Bugula neritina. Proteomics. 10:2972–2981. doi: 10.1002/pmic.201000056.10.1002/pmic.201000056
   PubMed Web of Science ®Google Scholar
• Wang KL, Zhang G, Sun J, Xu Y, Han Z, Liu LL, Shao CL, Liu QA, Wang CY, Qian PY. 2016. Cochliomycin A inhibits the larval settlement of Amphibalanus amphitrite by activating the NO/cGMP pathway. Biofouling. 32:35–44. doi: 10.1080/08927014.2015.1121245.10.1080/08927014.2015.1121245
   PubMed Web of Science ®Google Scholar
• Wendt DE. 1996. Effect of larval swimming duration on success of metamorphosis and size of the ancestrular lophophore in Bugula neritina (Bryozoa). Biol Bull. 191:224–233. doi: 10.2307/1542925.10.2307/1542925
   PubMed Web of Science ®Google Scholar
• Wendt DE, Woollacott RM. 1995. Induction of larval settlement by KCl in three species of Bugula (Bryozoa). Invertebr Biol. 114:345–351. doi: 10.2307/3226843.10.2307/3226843
   Web of Science ®Google Scholar
• Wong YH, Ryu T, Seridi L, Ghosheh Y, Bougouffa S, Qian PY, Ravasi T. 2014. Transcriptome analysis elucidates key developmental components of bryozoan lophophore development. Sci Rep. 4:6534.
   PubMed Web of Science ®Google Scholar
• Wong YH, Wang H, Ravasi T, Qian PY. 2012. Involvement of Wnt signaling pathways in the metamorphosis of the bryozoan Bugula neritina. Plos One. 7:e33323.
   PubMedGoogle Scholar
• Wood J, Garthwaite J. 1994. Models of the diffusional spread of nitric oxide: implications for neural nitric oxide signaling and its pharmacological properties. Neuropharmacology. 33:1235–1244. doi: 10.1016/0028-3908(94)90022-1.10.1016/0028-3908(94)90022-1
   PubMed Web of Science ®Google Scholar
• Woollacott RM, Zimmer RL. 1971. Attachment and metamorphosis of the cheilo-ctenostome bryozoan Bugula neritina (Linne). J Morphol(3). 134:351–382. doi: 10.1002/jmor.v134:3.10.1002/jmor.v134:3
   Web of Science ®Google Scholar
• Yamamoto H, Satuito CG, Yamazaki M, Natoyama K, Tachibana A, Fusetani N. 1998. Neurotransmitter blockers as antifoulants against planktonic larvae of the barnacle Balanus amphitrite and the mussel Mytilus galloprovincialis. Biofouling. 13:69–82. doi: 10.1080/08927019809378371.10.1080/08927019809378371
   Web of Science ®Google Scholar
• Yang JL, Glenn Satuito C, Bao WY, Kitamura H. 2008. Induction of metamorphosis of pediveliger larvae of the mussel Mytilus galloprovincialis Lamarck, 1819 using neuroactive compounds, KCl, NH4Cl and organic solvents. Biofouling. 24:461–470. doi: 10.1080/08927010802340309.10.1080/08927010802340309
   PubMed Web of Science ®Google Scholar
• Yang XX, Zhang Y, Wong YH, Qian, PY. 2018. HSP90 regulates larval settlement of the bryozoan Bugula neritina through NO pathway. J Experimental Biol. jeb-167478.
   Google Scholar
• Zhang G, He LS, Wong YH, Qian PY. 2013. MKK3 was involved in larval settlement of the barnacle Amphibalanus amphitrite through activating the kinase activity of p38MAPK. PLoS ONE. 8:e69510. doi: 10.1371/journal.pone.0069510.10.1371/journal.pone.0069510
   PubMed Web of Science ®Google Scholar
• Zhang Y, He LS, Zhang G, Xu Y, Lee OO, Matsumura K, Qian PY. 2012. The regulatory role of the NO/cGMP signal transduction cascade during larval attachment and metamorphosis of the barnacle Balanus (=Amphibalanus) amphitrite. J Exp Biol. 215:3813–3822. doi: 10.1242/jeb.070235.10.1242/jeb.070235
   PubMed Web of Science ®Google Scholar
• Zhang HM, Wong YH, Wang H, Chen ZF, Arellano SM, Ravasi T, Qian PY. 2011. Quantitative proteomics identify molecular targets that are crucial in larval settlement and metamorphosis of Bugula neritina. J Proteome Res. 10:340–360.
   Web of Science ®Google Scholar
• Zhao B, Zhang S, Qian PY. 2003. Larval settlement of the silver-or goldlip pearl oyster Pinctada maxima (Jameson) in response to natural biofilms and chemical cues. Aquaculture. 220:883–901. doi: 10.1016/S0044-8486(02)00567-7.10.1016/S0044-8486(02)00567-7
   Web of Science ®Google Scholar