Trauma-associated human neutrophil alterations revealed by comparative proteomics profiling

Jian Ying Zhou, Ravi K. Krovvidi, Yuqian Gao, Hong Gao, Brianne O. Petritis, Asit K. De, Carol L. Miller-Graziano, Paul E. Bankey, Vladislav A. Petyuk, Carrie D. Nicora, Therese R. Clauss, Ronald J. Moore, Tujin Shi, Joseph N. Brown, Amit Kaushal, Wenzhong Xiao, Ronald W. Davis, Ronald V. Maier, Ronald G. Tompkins, Wei Jun Qian & 38 others David G. Camp, Richard D. Smith, Henry V. Baker, Ulysses Balis, Timothy R. Billiar, Bernard H. Brownstein, Steven E. Calvano, Irshad H. Chaudry, J. Perren Cobb, Joseph Cuschieri, Bradley Freeman, Richard L. Gamelli, Nicole S. Gibran, Brian G. Harbrecht, Douglas L. Hayden, Laura Hennessy, Jureta W. Horton, Jeffrey Johnson, Matthew B. Klein, Stephen F. Lowry, John A. Mannick, Philip H. Mason, Grace P. McDonald-Smith, Michael N. Mindrinos, Joseph P. Minei, Ernest E. Moore, Avery B. Nathens, Grant E. O'Keefe, Laurence G. Rahme, Daniel G. Remick, David A. Schoenfeld, Michael B. Shapiro, Geoffrey M. Silver, John Storey, Robert Tibshirani, Mehmet Toner, H. Shaw Warren, Michael A. West

Research output: Contribution to journalArticle

12 Citations (Scopus)

Abstract

Purpose: Polymorphonuclear neutrophils (PMNs) play an important role in mediating the innate immune response after severe traumatic injury; however, the cellular proteome response to traumatic condition is still largely unknown. Experimental design: We applied 2D-LC-MS/MS-based shotgun proteomics to perform comparative proteome profiling of human PMNs from severe trauma patients and healthy controls. Results: A total of 197 out of ∼2500 proteins (being identified with at least two peptides) were observed with significant abundance changes following the injury. The proteomics data were further compared with transcriptomics data for the same genes obtained from an independent patient cohort. The comparison showed that the protein abundance changes for the majority of proteins were consistent with the mRNA abundance changes in terms of directions of changes. Moreover, increased protein secretion was suggested as one of the mechanisms contributing to the observed discrepancy between protein and mRNA abundance changes. Functional analyses of the altered proteins showed that many of these proteins were involved in immune response, protein biosynthesis, protein transport, NRF2-mediated oxidative stress response, the ubiquitin-proteasome system, and apoptosis pathways. Conclusions and clinical relevance: Our data suggest increased neutrophil activation and inhibited neutrophil apoptosis in response to trauma. The study not only reveals an overall picture of functional neutrophil response to trauma at the proteome level, but also provides a rich proteomics data resource of trauma-associated changes in the neutrophil that will be valuable for further studies of the functions of individual proteins in PMNs.

Original languageEnglish (US)
Pages (from-to)571-583
Number of pages13
JournalProteomics - Clinical Applications
Volume7
Issue number7-8
DOIs
StatePublished - Aug 2013

Fingerprint

Proteomics
Neutrophils
Wounds and Injuries
Proteins
Proteome
Apoptosis
Neutrophil Activation
Messenger RNA
Firearms
Protein Biosynthesis
Protein Transport
Proteasome Endopeptidase Complex
Ubiquitin
Innate Immunity
Oxidative stress
Biosynthesis
Oxidative Stress
Research Design
Design of experiments
Peptides

Keywords

  • Genomics
  • Human neutrophil
  • LC-MS/MS
  • Trauma

ASJC Scopus subject areas

  • Clinical Biochemistry

Cite this

Zhou, J. Y., Krovvidi, R. K., Gao, Y., Gao, H., Petritis, B. O., De, A. K., ... West, M. A. (2013). Trauma-associated human neutrophil alterations revealed by comparative proteomics profiling. Proteomics - Clinical Applications, 7(7-8), 571-583. https://doi.org/10.1002/prca.201200109

Trauma-associated human neutrophil alterations revealed by comparative proteomics profiling. / Zhou, Jian Ying; Krovvidi, Ravi K.; Gao, Yuqian; Gao, Hong; Petritis, Brianne O.; De, Asit K.; Miller-Graziano, Carol L.; Bankey, Paul E.; Petyuk, Vladislav A.; Nicora, Carrie D.; Clauss, Therese R.; Moore, Ronald J.; Shi, Tujin; Brown, Joseph N.; Kaushal, Amit; Xiao, Wenzhong; Davis, Ronald W.; Maier, Ronald V.; Tompkins, Ronald G.; Qian, Wei Jun; Camp, David G.; Smith, Richard D.; Baker, Henry V.; Balis, Ulysses; Billiar, Timothy R.; Brownstein, Bernard H.; Calvano, Steven E.; Chaudry, Irshad H.; Cobb, J. Perren; Cuschieri, Joseph; Freeman, Bradley; Gamelli, Richard L.; Gibran, Nicole S.; Harbrecht, Brian G.; Hayden, Douglas L.; Hennessy, Laura; Horton, Jureta W.; Johnson, Jeffrey; Klein, Matthew B.; Lowry, Stephen F.; Mannick, John A.; Mason, Philip H.; McDonald-Smith, Grace P.; Mindrinos, Michael N.; Minei, Joseph P.; Moore, Ernest E.; Nathens, Avery B.; O'Keefe, Grant E.; Rahme, Laurence G.; Remick, Daniel G.; Schoenfeld, David A.; Shapiro, Michael B.; Silver, Geoffrey M.; Storey, John; Tibshirani, Robert; Toner, Mehmet; Warren, H. Shaw; West, Michael A.

In: Proteomics - Clinical Applications, Vol. 7, No. 7-8, 08.2013, p. 571-583.

Research output: Contribution to journalArticle

Zhou, JY, Krovvidi, RK, Gao, Y, Gao, H, Petritis, BO, De, AK, Miller-Graziano, CL, Bankey, PE, Petyuk, VA, Nicora, CD, Clauss, TR, Moore, RJ, Shi, T, Brown, JN, Kaushal, A, Xiao, W, Davis, RW, Maier, RV, Tompkins, RG, Qian, WJ, Camp, DG, Smith, RD, Baker, HV, Balis, U, Billiar, TR, Brownstein, BH, Calvano, SE, Chaudry, IH, Cobb, JP, Cuschieri, J, Freeman, B, Gamelli, RL, Gibran, NS, Harbrecht, BG, Hayden, DL, Hennessy, L, Horton, JW, Johnson, J, Klein, MB, Lowry, SF, Mannick, JA, Mason, PH, McDonald-Smith, GP, Mindrinos, MN, Minei, JP, Moore, EE, Nathens, AB, O'Keefe, GE, Rahme, LG, Remick, DG, Schoenfeld, DA, Shapiro, MB, Silver, GM, Storey, J, Tibshirani, R, Toner, M, Warren, HS & West, MA 2013, 'Trauma-associated human neutrophil alterations revealed by comparative proteomics profiling', Proteomics - Clinical Applications, vol. 7, no. 7-8, pp. 571-583. https://doi.org/10.1002/prca.201200109
Zhou, Jian Ying ; Krovvidi, Ravi K. ; Gao, Yuqian ; Gao, Hong ; Petritis, Brianne O. ; De, Asit K. ; Miller-Graziano, Carol L. ; Bankey, Paul E. ; Petyuk, Vladislav A. ; Nicora, Carrie D. ; Clauss, Therese R. ; Moore, Ronald J. ; Shi, Tujin ; Brown, Joseph N. ; Kaushal, Amit ; Xiao, Wenzhong ; Davis, Ronald W. ; Maier, Ronald V. ; Tompkins, Ronald G. ; Qian, Wei Jun ; Camp, David G. ; Smith, Richard D. ; Baker, Henry V. ; Balis, Ulysses ; Billiar, Timothy R. ; Brownstein, Bernard H. ; Calvano, Steven E. ; Chaudry, Irshad H. ; Cobb, J. Perren ; Cuschieri, Joseph ; Freeman, Bradley ; Gamelli, Richard L. ; Gibran, Nicole S. ; Harbrecht, Brian G. ; Hayden, Douglas L. ; Hennessy, Laura ; Horton, Jureta W. ; Johnson, Jeffrey ; Klein, Matthew B. ; Lowry, Stephen F. ; Mannick, John A. ; Mason, Philip H. ; McDonald-Smith, Grace P. ; Mindrinos, Michael N. ; Minei, Joseph P. ; Moore, Ernest E. ; Nathens, Avery B. ; O'Keefe, Grant E. ; Rahme, Laurence G. ; Remick, Daniel G. ; Schoenfeld, David A. ; Shapiro, Michael B. ; Silver, Geoffrey M. ; Storey, John ; Tibshirani, Robert ; Toner, Mehmet ; Warren, H. Shaw ; West, Michael A. / Trauma-associated human neutrophil alterations revealed by comparative proteomics profiling. In: Proteomics - Clinical Applications. 2013 ; Vol. 7, No. 7-8. pp. 571-583.
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abstract = "Purpose: Polymorphonuclear neutrophils (PMNs) play an important role in mediating the innate immune response after severe traumatic injury; however, the cellular proteome response to traumatic condition is still largely unknown. Experimental design: We applied 2D-LC-MS/MS-based shotgun proteomics to perform comparative proteome profiling of human PMNs from severe trauma patients and healthy controls. Results: A total of 197 out of ∼2500 proteins (being identified with at least two peptides) were observed with significant abundance changes following the injury. The proteomics data were further compared with transcriptomics data for the same genes obtained from an independent patient cohort. The comparison showed that the protein abundance changes for the majority of proteins were consistent with the mRNA abundance changes in terms of directions of changes. Moreover, increased protein secretion was suggested as one of the mechanisms contributing to the observed discrepancy between protein and mRNA abundance changes. Functional analyses of the altered proteins showed that many of these proteins were involved in immune response, protein biosynthesis, protein transport, NRF2-mediated oxidative stress response, the ubiquitin-proteasome system, and apoptosis pathways. Conclusions and clinical relevance: Our data suggest increased neutrophil activation and inhibited neutrophil apoptosis in response to trauma. The study not only reveals an overall picture of functional neutrophil response to trauma at the proteome level, but also provides a rich proteomics data resource of trauma-associated changes in the neutrophil that will be valuable for further studies of the functions of individual proteins in PMNs.",
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TY - JOUR

T1 - Trauma-associated human neutrophil alterations revealed by comparative proteomics profiling

AU - Zhou, Jian Ying

AU - Krovvidi, Ravi K.

AU - Gao, Yuqian

AU - Gao, Hong

AU - Petritis, Brianne O.

AU - De, Asit K.

AU - Miller-Graziano, Carol L.

AU - Bankey, Paul E.

AU - Petyuk, Vladislav A.

AU - Nicora, Carrie D.

AU - Clauss, Therese R.

AU - Moore, Ronald J.

AU - Shi, Tujin

AU - Brown, Joseph N.

AU - Kaushal, Amit

AU - Xiao, Wenzhong

AU - Davis, Ronald W.

AU - Maier, Ronald V.

AU - Tompkins, Ronald G.

AU - Qian, Wei Jun

AU - Camp, David G.

AU - Smith, Richard D.

AU - Baker, Henry V.

AU - Balis, Ulysses

AU - Billiar, Timothy R.

AU - Brownstein, Bernard H.

AU - Calvano, Steven E.

AU - Chaudry, Irshad H.

AU - Cobb, J. Perren

AU - Cuschieri, Joseph

AU - Freeman, Bradley

AU - Gamelli, Richard L.

AU - Gibran, Nicole S.

AU - Harbrecht, Brian G.

AU - Hayden, Douglas L.

AU - Hennessy, Laura

AU - Horton, Jureta W.

AU - Johnson, Jeffrey

AU - Klein, Matthew B.

AU - Lowry, Stephen F.

AU - Mannick, John A.

AU - Mason, Philip H.

AU - McDonald-Smith, Grace P.

AU - Mindrinos, Michael N.

AU - Minei, Joseph P.

AU - Moore, Ernest E.

AU - Nathens, Avery B.

AU - O'Keefe, Grant E.

AU - Rahme, Laurence G.

AU - Remick, Daniel G.

AU - Schoenfeld, David A.

AU - Shapiro, Michael B.

AU - Silver, Geoffrey M.

AU - Storey, John

AU - Tibshirani, Robert

AU - Toner, Mehmet

AU - Warren, H. Shaw

AU - West, Michael A.

PY - 2013/8

Y1 - 2013/8

N2 - Purpose: Polymorphonuclear neutrophils (PMNs) play an important role in mediating the innate immune response after severe traumatic injury; however, the cellular proteome response to traumatic condition is still largely unknown. Experimental design: We applied 2D-LC-MS/MS-based shotgun proteomics to perform comparative proteome profiling of human PMNs from severe trauma patients and healthy controls. Results: A total of 197 out of ∼2500 proteins (being identified with at least two peptides) were observed with significant abundance changes following the injury. The proteomics data were further compared with transcriptomics data for the same genes obtained from an independent patient cohort. The comparison showed that the protein abundance changes for the majority of proteins were consistent with the mRNA abundance changes in terms of directions of changes. Moreover, increased protein secretion was suggested as one of the mechanisms contributing to the observed discrepancy between protein and mRNA abundance changes. Functional analyses of the altered proteins showed that many of these proteins were involved in immune response, protein biosynthesis, protein transport, NRF2-mediated oxidative stress response, the ubiquitin-proteasome system, and apoptosis pathways. Conclusions and clinical relevance: Our data suggest increased neutrophil activation and inhibited neutrophil apoptosis in response to trauma. The study not only reveals an overall picture of functional neutrophil response to trauma at the proteome level, but also provides a rich proteomics data resource of trauma-associated changes in the neutrophil that will be valuable for further studies of the functions of individual proteins in PMNs.

AB - Purpose: Polymorphonuclear neutrophils (PMNs) play an important role in mediating the innate immune response after severe traumatic injury; however, the cellular proteome response to traumatic condition is still largely unknown. Experimental design: We applied 2D-LC-MS/MS-based shotgun proteomics to perform comparative proteome profiling of human PMNs from severe trauma patients and healthy controls. Results: A total of 197 out of ∼2500 proteins (being identified with at least two peptides) were observed with significant abundance changes following the injury. The proteomics data were further compared with transcriptomics data for the same genes obtained from an independent patient cohort. The comparison showed that the protein abundance changes for the majority of proteins were consistent with the mRNA abundance changes in terms of directions of changes. Moreover, increased protein secretion was suggested as one of the mechanisms contributing to the observed discrepancy between protein and mRNA abundance changes. Functional analyses of the altered proteins showed that many of these proteins were involved in immune response, protein biosynthesis, protein transport, NRF2-mediated oxidative stress response, the ubiquitin-proteasome system, and apoptosis pathways. Conclusions and clinical relevance: Our data suggest increased neutrophil activation and inhibited neutrophil apoptosis in response to trauma. The study not only reveals an overall picture of functional neutrophil response to trauma at the proteome level, but also provides a rich proteomics data resource of trauma-associated changes in the neutrophil that will be valuable for further studies of the functions of individual proteins in PMNs.

KW - Genomics

KW - Human neutrophil

KW - LC-MS/MS

KW - Trauma

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