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Quantitative Proteomics Reveals Manganese Alleviates Heat Stress of Broiler Myocardial Cells via Regulating Nucleic Acid Metabolism

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Abstract

Heat stress threatens severely cardiac function by caused myocardial injury in poultry. Our previous study has showed that manganese (Mn) has a beneficial effect on heat-stress resistance of broiler. Therefore, we tried to confirm the alleviation mechanism through proteomic analysis after heat stress exposure to primary broiler myocardial cells pretreated with Mn. The experiment was divided into four groups: CON group (37 °C, cells without any treatment), HS group (43 °C, cells treatment with heat stress for 4 h), HS+MnCl2 group (cells treated with 20 μM MnCl2 before heat stress), and HS+Mn-AA group (cells treated with 20 μM Mn compound amino acid complex before heat stress). Proteome analysis using DIA identified 300 differentially expressed proteins (DEPs) between CON group and HS group; 93 and 121 DEPs were identified in inorganic manganese treatment group and organic manganese treatment group, respectively; in addition, there were 53 DEPs identified between inorganic and organic manganese group. Gene Ontology (GO) analysis showed that DEPs were mainly involved in binding, catalytic activity, response to stimulus, and metabolic process. DEPs of manganese pretreatment involved in a variety of biological regulatory pathways, and significantly influenced protein processing and repair in endoplasmic reticulum, apoptosis, and DNA replication and repair. These all seem to imply that manganese may help to resist cell damage induced by heat stress by regulating key node proteins. These findings contribute to a better understanding of the effects of manganese on overall protein changes during heat-stress and the possible mechanisms, as well as how to better use manganese to protect heart function in high temperature.

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References

  1. Jahejo AR, Rajput N, Rajput NM, Leghari IH, Kaleri RR, Mangi RA, Sheikh MK, Pirzado MZ (2016) Effects of heat stress on the performance of Hubbard broiler chicken. Cells 2:1–5

    Google Scholar 

  2. Zaboli GR, Rahimi S, Shariatmadari F, Torshizi MAK, Baghbanzadeh A, Mehri M (2017) Thermal manipulation during pre and post-hatch on thermotolerance of male broiler chickens exposed to chronic heat stress. Poult Sci 96(2):478–485. https://doi.org/10.3382/ps/pew344

    Article  CAS  PubMed  Google Scholar 

  3. Kamel NN, Ahmed AMH, Mehaisen GMK, Mashaly MM, Abass AO (2017) Depression of leukocyte protein synthesis, immune function and growth performance induced by high environmental temperature in broiler chickens. Int J Biometeorol 61(9):1637–1645. https://doi.org/10.1007/s00484-017-1342-0

    Article  PubMed  Google Scholar 

  4. St-Pierre NR, Cobanov B, Schnitkey G (2003) Economic losses from heat stress by US livestock industries. J Dairy Sci 86:E52–E77. https://doi.org/10.3168/jds.S0022-0302(03)74040-5

    Article  Google Scholar 

  5. Chang CP, Hsu YC, Lin MT (2003) Magnolol protects against cerebral ischaemic injury of rat heatstroke. Clin Exp Pharmacol P 30(5-6):387–392. https://doi.org/10.1046/j.1440-1681.2003.03847.x

    Article  CAS  Google Scholar 

  6. Wu D, Xu J, Song E, Tang S, Zhang XH, Kemper N, Hartung J, Bao E (2015) Acetyl salicylic acid protected against heat stress damage in chicken myocardial cells and may associate with induced Hsp27 expression. Cell Stress Chaperon 20(4):687–696. https://doi.org/10.1007/s12192-015-0596-x

    Article  CAS  Google Scholar 

  7. Xu Y, Jie Z, Lin L, Bo Y, Chen BX, Bao ED, Zhang XH (2023) Hsp90 protected chicken primary myocardial cells from heat-stress injury by inhibiting oxidative stress and calcium overload in mitochondria. Biochem Pharmacol 209:115434

    Article  Google Scholar 

  8. Yang L, Tan GY, Fu YQ, Feng JH, Zhang MH (2010) Effects of acute heat stress and subsequent stress removal on function of hepatic mitochondrial respiration, ROS production and lipid peroxidation in broiler chickens. Comp Biochem Phys C 151(2):204–208. https://doi.org/10.1016/j.cbpc.2009.10.010

    Article  CAS  Google Scholar 

  9. Slimen IB, Najar T, Ghram A, Dabbebi H, Mrad MB, Abdrabbah M (2014) Reactive oxygen species, heart stress and oxidative-induced mitoehondrial damage. A review Int J Hyperther 30(7):513–523. https://doi.org/10.3109/02656736.2014.971446

    Article  CAS  Google Scholar 

  10. Gu XH, Hao Y, Wang XL (2012) Overexpression of heat shock protein 70 and its relationship to intestine under acute heat stress in broilers: 2 intestinal oxidative stress. Poultry Sci 91(4):790–799. https://doi.org/10.3382/ps.2011-01628

    Article  CAS  Google Scholar 

  11. Víctor MV, Milagros R, Mónica DLF (2003) Regulation of macrophage function by the antioxidant N-acetylcysteine in mouse-oxidative stress by endotoxin. Int Immunopharmacol 3(1):97–106. https://doi.org/10.1016/s1567-5769(02)00232-1

    Article  PubMed  Google Scholar 

  12. Zeng T, Li JJ, Wang DQ, Li GQ, Wang GL, Lu LZ (2014) Effects of heat stress on antioxidant defense system, inflammatory injury, and heat shock proteins of Muscovy and Pekin ducks: evidence for differential thermal sensitivities. Cell Stress Chaperon 19(6):895–901. https://doi.org/10.1007/s12192-014-0514-7

    Article  CAS  Google Scholar 

  13. Zhu YE, Lu L, Liao XD, Li WX, Zhang LY, Ji C, Lin X, Liu HC, Jack O, Luo XG (2017) Maternal dietary manganese protects chick embryos against maternal heat stress via epigenetic-activated antioxidant and antiapoptotic abilities. Oncotarget 8(52):89665–89680. https://doi.org/10.18632/oncotarget.20804

    Article  PubMed  PubMed Central  Google Scholar 

  14. Li SF, Lu L, Liao XD, Gao TQ, Wang F, Zhang LY, Xi L, Liu SB, Luo XG (2016) Manganese elevates manganese superoxide dismutase protein level through protein kinase C and protein tyrosine kinase. Biometals 29(2):265–274. https://doi.org/10.1007/s10534-016-9913-9

    Article  CAS  PubMed  Google Scholar 

  15. Qin SZ, Huang L, Lu L, Zhang LY, Guo YL, Xi L, Liao XD, Luo XG (2023) Manganese alleviates heat stress of primary cultured chick embryonic myocardial cells via enhancing manganese superoxide dismutase expression and attenuating heat shock response. J Therm Biol 112:103440

    Article  CAS  PubMed  Google Scholar 

  16. Liao XD, Zhu YW, Lu L, Li WX, Zhang LY, Ji C, Lin X, Luo XG (2019) Maternal manganese activates anti-apoptotic-related gene expressions via miR-1551 and miR-34c in embryonic hearts from maternal heat stress (Gallus gallus). J Therm Biol 84:190–199. https://doi.org/10.1016/j.jtherbio.2019.07.014

    Article  CAS  PubMed  Google Scholar 

  17. Monti C, Zilocchi M, Colugnat I, Alberio T (2019) Proteomics turns functional. J Proteomics 198:36–44. https://doi.org/10.1016/j.jprot.2018.12.012

    Article  CAS  PubMed  Google Scholar 

  18. Allison D (2015) DIA mass spectrometry. Nat Methods 12(1):35–35. https://doi.org/10.1038/nmeth.3234

    Article  CAS  Google Scholar 

  19. Vidova V, Spacil Z (2017) A review on mass spectrometry-based quantitative proteomics: targeted and data independent acquisition. Anal Chim Acta 964:7–23. https://doi.org/10.1016/j.aca.2017.01.059

    Article  CAS  PubMed  Google Scholar 

  20. Floriou-Servou A, Lukas VZ, Luzia S, Oliver S, Mattia P, Anahita R, Alessio C, Beat T, Johannes B (2018) Distinct proteomic, transcriptomic and epigenetic stress-responses in dorsal and ventral hippocampus. Biol Psychiat 84(7):531–541. https://doi.org/10.1016/j.biopsych.2018.02.003

    Article  CAS  PubMed  Google Scholar 

  21. Horning KJ, Caito SW, Tipps KG, Bowman AB, Aschner M (2015) Manganese is essential for neuronal health. Annu Rev Nutr 35:71–108. https://doi.org/10.1146/annurev-nutr-071714-034419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Gunter EJM Gavin CE, Aschner M Thomas EG (2013) Manganese neurotoxicity and the role of reactive oxygen species. Free Radical Bio Med 62:65-75. https://doi.org/10.1016/j.freeradbiomed.2013.01.032.

  23. Lopez V, Heijden EVD, Villar M, Michel A, Alberdi P, Gortázar C, Rutten V, Fuente JDL (2018) Comparative proteomics identified immune response proteins involved in response to vaccination with heat-inactivated Mycobacterium bovis and mycobacterial challenge in cattle. Vet Immunol Immunop 206:54–64. https://doi.org/10.1016/j.vetimm.2018.10.013

    Article  CAS  Google Scholar 

  24. Matsuki SG, Iuchi Y, Ikeda Y, Sasagawa I, Tomita Y, Fujii J (2003) Suppression of cytochrome c release and apoptosis in testes with heat stress by minocycline. Biochem Bioph Res Co 312(3):843–849. https://doi.org/10.1016/j.bbrc.2003.10.191

    Article  CAS  Google Scholar 

  25. Saelao P, Wang Y, Chanthavixay G, Yu V, Gallardo RA, Dekkers JM (2018) Integrated proteomic and transcriptomic analysis of differential expression of chicken lung tissue in response to NDV infection during heat stress. Genes-Basel 9(12):579. https://doi.org/10.3390/genes9120579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Ari M,and Hrusti O (1975) Exposure to airborne manganese and arterial blood pressure. Environ Res 10(2):314-318. https://doi.org/10.1016/0013-9351(75)90092-4.

    Article  Google Scholar 

  27. Meares GP, Zmijewska AA, Jope RS (2004) Heat shock protein-90 dampens and directs signaling stimulated by insulin-like growth factor-1 and insulin. FEBS Lett 574(1-3):181–186. https://doi.org/10.1016/j.febslet.2004.08.026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Langer T, Neupert W (1991) Heat shock proteins hsp60 and hsp70: their roles in folding, assembly and membrane translocation of proteins. Curr Top Microbiol 167:3–30. https://doi.org/10.1007/978-3-642-75875-1_1

    Article  CAS  Google Scholar 

  29. Fang X, Bogomolovas J, Trexler C, Chen J (2019) The BAG3-dependent and -independent roles of cardiac small heat shock proteins. JCI Insight 4(4):e126464. https://doi.org/10.1172/jci.insight.126464

    Article  PubMed  PubMed Central  Google Scholar 

  30. Carra S, Simon A, Arrigo PA, Benesch JL, Benjamin IJ (2017) The growing world of small heat shock proteins: from structure to functions. Cell Stress Chaperon 22(4):601–611. https://doi.org/10.1007/s12192-017-0787-8

    Article  CAS  Google Scholar 

  31. Mymrikov EV, Daake M, Richter B, Haslbeck M, Buchner J (2017) The chaperone activity and substrate spectrum of human small heat shock proteins. J Biol Chem 292(2):672–684. https://doi.org/10.1074/jbc.M116.760413

    Article  CAS  PubMed  Google Scholar 

  32. Depre C, Hase M, Gaussin V, Zajac A, Wang L, Hittinger L, Ghaleh B, Yu XZ, Kudej RK, Wagner T, Sadoshima J, Vatner SF (2002) H11 kinase is a novel mediator of myocardial hypertrophy in vivo. Circ Res 91(11):1007–1014. https://doi.org/10.1161/01.RES.0000044380.54893.4B

    Article  CAS  PubMed  Google Scholar 

  33. Rauch JN, Tse E, Freilich R, Mok SA, Makley LN, Southworth DR, Gestwicki JE (2017) BAG3 is a modular, scaffolding protein that physically links heat shock protein 70 (Hsp70) to the small heat shock proteins. J Mol Cell Biol 429(1):128–141. https://doi.org/10.1016/j.jmb.2016.11.013

    Article  CAS  Google Scholar 

  34. Verschuure P, Tatard C, Boelens WC, Grongnet JF, David JC (2003) Expression of small heat shock proteins HspB2, HspB8, Hsp20 and cvHsp in different tissues of the perinatal developing pig. Eur J Cell Biol 82(10):523–530. https://doi.org/10.1078/0171-9335-00337

    Article  CAS  PubMed  Google Scholar 

  35. Carra S, Seguin SJ, Landry J (2008) HspB8 and Bag3: a new chaperone complex targeting misfolded proteins to macroautophagy. Autophagy 4(2):237–239. https://doi.org/10.4161/auto.5407

    Article  CAS  PubMed  Google Scholar 

  36. Li FZ, Xiao H, Hu ZP, Zhou FF, Yang BB (2018) Exploring the multifaceted roles of heat shock protein B8 (HSPB8) in diseases. Eur J Cell Biol 97(3):216–229. https://doi.org/10.1016/j.ejcb.2018.03.003

    Article  CAS  PubMed  Google Scholar 

  37. Guilbert SM, Lambert H, Rodrigue MA, Fuchs M, Landry J, Lavoie JN (2018) HSPB8 and BAG3 cooperate to promote spatial sequestration of ubiquitinated proteins and coordinate the cellular adaptive response to proteasome insufficiency. Faseb J 32(7):3518–3535. https://doi.org/10.1096/fj.201700558RR

    Article  CAS  PubMed  Google Scholar 

  38. Mehlen P, Mehlen A, Godet J, Arrigo AP (1997) Hsp27 as a switch between differentiation and apoptosis in murine embryonic stem cells. J Biol Chem 272(50):31657–31665. https://doi.org/10.1074/jbc.272.50.31657

    Article  CAS  PubMed  Google Scholar 

  39. Doong H, Vrailas A, Kohn EC (2002) What’s in the ‘BAG’?–a functional domain analysis of the BAG-family proteins. Cancer Lett 188(1-2):25–32. https://doi.org/10.1016/s0304-3835(02)00456-1

    Article  CAS  PubMed  Google Scholar 

  40. Festa M, Valle LD, Khalili K, Franco R, Scognamiglio G, Graziano V, Laurenzi VD, Turco MC, Rosati A (2011) BAG3 protein is overexpressed in human glioblastoma and is a potential target for its therapy. Am J Surg Pathol 178(6):2504–2512. https://doi.org/10.1016/j.ajpath.2011.02.002

    Article  CAS  Google Scholar 

  41. Rosati A, Graziano V, Laurenzi VD, Pascale M, Turco MC (2011) BAG3: a multifaceted protein that regulates major cell pathway. Cell Death Dis 2(4):e141. https://doi.org/10.1038/cddis.2011.24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett DR, Aebersold R, Siderovski DP, Penninger JM, Kroemer G (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397(6718):441–446. https://doi.org/10.1038/17135

    Article  CAS  PubMed  Google Scholar 

  43. Joza N, Susin SA, Daugas E, Stanford WL, Cho SK (2001) Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature 410(6828):549–554. https://doi.org/10.1038/35069004

    Article  CAS  PubMed  Google Scholar 

  44. Norberg E, Orrenius S, Zhivotovsky B (2010) Mitochondrial regulation of cell death: processing of apoptosis-inducing factor (AIF). Biochem Bioph Res Co 396(1):95–100. https://doi.org/10.1016/j.bbrc.2010.02.163

    Article  CAS  Google Scholar 

  45. Bonora M, Pedro JMB, Kroemer G, Galluzzi L, Pinton P (2014) Novel insights into the mitochondrial permeability transition. Cell Cycle. 13(17):2666–2670. https://doi.org/10.4161/15384101.2014.949082

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Qin SZ, Wang R, Tang DF, Qin SJ, Guo YL, Shi ZG (2022) Manganese mitigates heat stress-induced apoptosis by alleviating endoplasmic reticulum stress and activating the NRF2/SOD2 pathway in primary chick embryonic myocardial cells. Biol Trace Elem Res 200:2312–2320. https://doi.org/10.1007/s12011-021-02810-2

    Article  CAS  PubMed  Google Scholar 

  47. Wang R, Shi ZG, Li JL, Tang DF, Qin SZ, Guo YL (2022) Protective effect of manganese on apoptosis and mitochondrial function of heat-stressed primary chick embryonic myocardial cells. Biol Trace Elem Res 200:4419–4429. https://doi.org/10.1007/s12011-021-03016-2

    Article  CAS  PubMed  Google Scholar 

  48. Kaufmann T, Schlipf S, Sanz J, Neubert K, Stein R, Borner C (2003) Characterization of the signal that directs Bcl-x[sub L], but not Bcl-2, to the mitochondrial outer membrane. J Mol Cell Biol 160(1):53–64. https://doi.org/10.1083/jcb.200210084

    Article  CAS  Google Scholar 

  49. Iftode C, Daniely Y, Borowiec JA (1999) Replication protein A (RPA): the eukaryotic SSB. Crit Rev Biochem Mol 34(3):141–180. https://doi.org/10.1080/10409239991209255

    Article  CAS  Google Scholar 

  50. Burns JL, Guzder SN, Sung P, Prakash S, Prakash L (1996) An affinity of human replication protein A for ultraviolet-damaged DNA. J Biol Inorg Chem 271(20):11607–11610. https://doi.org/10.1074/jbc.271.20.11607

    Article  CAS  Google Scholar 

  51. Costa RMA, Chiganças V, Galhardo RDS, Carvalho H, Menck CFM (2003) The eukaryotic nucleotide excision repair pathway. Biochimie 85(11):1083–1099. https://doi.org/10.1016/j.biochi.2003.10.017

    Article  CAS  PubMed  Google Scholar 

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Funding

This research was funded by the National Natural Science Foundation of China (No. 31960668) and Discipline Team Project of Gansu Agricultural University (NO: GAU-XKTD-2022-24).

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Shizhen Qin: conceptualization, methodology, writing—original draft preparation; Rui Wang: conceptualization, methodology, software; Jinlu Li: contributed materials, data curation, methodology; Defu Tang: methodology, software; Zhaoguo Shi: project administration, methodology.

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Correspondence to Zhaoguo Shi.

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Qin, S., Wang, R., Li, J. et al. Quantitative Proteomics Reveals Manganese Alleviates Heat Stress of Broiler Myocardial Cells via Regulating Nucleic Acid Metabolism. Biol Trace Elem Res 202, 1187–1202 (2024). https://doi.org/10.1007/s12011-023-03731-y

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