Chapter 7 : Immune Defense at Mucosal Surfaces

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Immune Defense at Mucosal Surfaces, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555816872/9781555815141_Chap07-1.gif /docserver/preview/fulltext/10.1128/9781555816872/9781555815141_Chap07-2.gif


The mucosal surfaces of the body together represent a vast surface area separated from the outside world only by delicate epithelial barriers. Isolated lymphoid follicles (ILFs) are common at mucocutaneous transitions such as the anal-rectal junction and near the ducts of secretory glands that empty onto mucosal surfaces. Most mucosal cells involved in immune defense are distributed diffusely throughout the subepithelial connective tissue and are directly or indirectly responsible for immune effector functions. Induction of mucosal immune responses is complicated by the fact that antigens and microorganisms on mucosal surfaces are separated from cells of the mucosal immune system by epithelial barriers. Infection of local target cells and dissemination of virus to regional lymph nodes and other tissues occur rapidly after deposition of virus on mucosal surfaces. Five to seven days are required for initial induction in organized mucosal lymphoid tissues, directed migration, and terminal differentiation of cells in widespread mucosal sites. B cells from Peyer's patches and other organized mucosa-associated lymphoid tissues (MALT) complete their differentiation only after arrival in the lamina propria. Responses to mucosal vaccines are greatly amplified by local boosts, due to the abundant populations of memory T and B cells in mucosal tissues that allow for local amplification of effector responses on reexposure to an antigen. Local exposure to an antigen and/or adjuvant evokes cytokines and chemokines from epithelia, DCs, and other cells and up-regulates expression of addressins on local endothelia, increasing the numbers and enhancing the functions of mucosal effector cells.

Citation: Neutra M, Kraehenbuhl J. 2011. Immune Defense at Mucosal Surfaces, p 97-107. In Kaufmann S, Rouse B, Sacks D (ed), The Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555816872.ch7
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of FIGURE 1

Antigen sampling across epithelial barriers. Antigen sampling strategies at mucosal surfaces involve collaborations between epithelial and dendritic cells (DCs). The diverse mechanisms involved are adapted to the nature of the local epithelial barrier. At most mucosal surfaces where the epithelium is stratified, pseudostratified, or simple columnar, DCs are stationed immediately under the epithelium, migrate into the epithelial layer, and may extend dendrites into the lumen to capture antigens. These DCs generally travel to the nearest draining lymph node to present antigen to T cells. At sites of organized mucosal lymphoid tissues, specialized M cells in the lymphoid follicle-associated epithelium deliver antigens by transcytosis across the epithelial barrier, directly to intraepithelial and subepithelial DCs. These DCs then migrate to adjacent mucosal T-cell areas to present antigen. (Reproduced from ).

Citation: Neutra M, Kraehenbuhl J. 2011. Immune Defense at Mucosal Surfaces, p 97-107. In Kaufmann S, Rouse B, Sacks D (ed), The Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555816872.ch7
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2

Mechanisms of immune protection at mucosal surfaces. Mucosal immune protection depends on the contributions of multiple cell types. Antigen-specific effector B and T cells that bear mucosal homing receptors recognize addressins on mucosal high endothelial venules and enter the mucosa. In response to epithelial and dendritic cell signals, the B cells terminally differentiate to become mucosal plasma cells. Most plasma cells produce dimeric IgA that is exported into secretions as S-IgA to intercept antigens and pathogens and prevent mucosal invasion. IgA, as well as IgG from local plasma cells or blood, can also neutralize pathogens within the mucosa. Local cytotoxic T cells and antibodies collaborate to kill infected cells. Pathogens are also captured by dendritic cells (DC) and macrophages (Mf), and carried to draining lymph nodes. (Reproduced from ).

Citation: Neutra M, Kraehenbuhl J. 2011. Immune Defense at Mucosal Surfaces, p 97-107. In Kaufmann S, Rouse B, Sacks D (ed), The Immune Response to Infection. ASM Press, Washington, DC. doi: 10.1128/9781555816872.ch7
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Agace, W. W.,, J. M. Higgins,, B. Sadasivan,, M. B. Brenner, and, C. M. Parker. 2000. T-lymphocyte-epithelial-cell interactions: integrin alpha(E)(CD103)beta(7), LEEP-CAM and chemokines. Curr. Opin. Cell Biol. 12: 563568.
2. Anderle, P.,, M. Rumbo,, F. Sierro,, R. Mansourian,, P. Michetti,, M. Roberts, and, J. P. Kraehenbuhl. 2005. Novel markers of the human follicle-associated epithelium identified by genomic profiling and microdissection. Gastroenterology 129: 321327.
3. Backhed, F.,, R. E. Ley,, J. L. Sonnenburg,, D. A. Peterson, and, J. I. Gordon. 2005. Host-bacterial mutualism in the human intestine. Science 307: 19151920.
4. Belyakov, I. M., and, J. D. Ahlers. 2008. Functional CD8+ CTLs in mucosal sites and HIV infection: moving forward toward a mucosal AIDS vaccine. Trends Immunol. 29: 574585.
5. Bergtold, A.,, D. D. Desai,, A. Gavhane, and, R. Clynes. 2005. Cell surface recycling of internalized antigen permits dendritic cell priming of B cells. Immunity 23: 503514.
6. Bevins, C. L. 2006. Paneth cell defensins: key effector molecules of innate immunity. Biochem. Soc. Trans. 34: 263266.
7. Bienenstock, J., and, R. L. Clancy. 2005. Bronchus-associated lymphoid tissues, p. 375–384. In J. Mestecky,, J. Bienenstock,, M. Lamm,, L. Mayer,, J. McGhee, and, W. Strober (ed.), Mucosal Immunology, 3rd ed. Academic Press, San Diego, CA.
8. Brandtzaeg, P.,, H. S. Carlsen, and, I. N. Farstad. 2005. The human mucosal B cell system. p. 617–654. In J. Mestecky,, J. Bienenstock,, M. Lamm,, L. Mayer,, J. McGhee, and, W. Strober (eds.), Mucosal Immunology, 3rd ed. Academic Press, San Diego, CA.
9. Brenchley, J. M., and, D. C. Douek. 2008. HIV infection and the gastrointestinal immune system. Mucosal Immunol. 1: 2330.
10. Cerutti, A. 2008. The regulation of IgA class switching. Nat. Rev. Immunol. 8: 421434.
11. Chabot, S. M.,, M. Shawi,, T. Eaves-Pyles, and, M. R. Neutra. 2008. Flagellin modulates functions of the follicle-associated epithelium to facilitate uptake of particles into organized mucosal lymphoid tissues. J. Infect. Dis. 198: 907910.
12. Cohen, N. R.,, S. Garg, and, M. B. Brenner. 2009. Antigen presentation by CD1 lipids, T cells, and NKT cells in microbial immunity. Adv. Immunol. 102: 194.
13. Cone, R. A. 2005. Mucus. p. 49–72. In J. Mestecky,, J. Bienenstock,, M. Lamm,, L. Mayer,, J. McGhee, and, W. Strober (ed.), Mucosal Immunology, 3rd ed. Academic Press, San Diego, CA.
14. Coombes, J. L., and, F. Powrie. 2008. Dendritic cells in intestinal immune regulation. Nat. Rev. Immunol. 8: 435446.
15. Corbett, M.,, W. M. Bogers,, J. L. Heeney,, S. Gerber,, C. Genin,, A. Didierlaurent,, H. Oostermeijer,, R. Dubbes,, G. Braskamp,, S. Lerondel,, C. E. Gomez,, M. Esteban,, R. Wagner,, I. Kondova,, P. Mooij,, S. Balla-Jhagjhoorsingh,, N. Beenhakker,, G. Koopman,, S. van der Burg,, J. P. Kraehenbuhl, and, A. Le Pape. 2008. Aerosol immunization with NYVAC and MVA vectored vaccines is safe, simple, and immunogenic. Proc. Natl. Acad. Sci. USA 105: 20462051.
16. Das, G., and, C. A. Janeway, Jr. 2003. MHC specificity of iIELs. Trends Immunol. 24: 8893.
17. Debard, N.,, F. Sierro,, J. Browning, and, J. P. Kraehenbuhl. 2001. Effect of mature lymphocytes and lymphotoxin on the development of the follicle-associated epithelium and M cells in mouse Peyer’s patches. Gastroenterology 120: 11731182.
18. Ellermeier, J. R., and, J. M. Slauch. 2007. Adaptation to the host environment: regulation of the SPI1 type III secretion system in Salmonella enterica serovar Typhimurium. Curr. Opin. Microbiol. 10: 2429.
19. Elson, C. O.,, and M. T. Dertzbaugh. 2005. Mucosal adjuvants, p. 967–986. In J. Mestecky,, J. Bienenstock,, M. Lamm,, L. Mayer,, J. McGhee, and, W. Strober (ed.), Mucosal Immunology, 3rd ed. Academic Press, San Diego, CA.
20. Fagarasan, S., and, T. Honjo. 2003. Intestinal IgA synthesis: regulation of front-line body defences. Nat. Rev. Immunol. 3: 6372.
21. Faria, A.M., and, H. L. Weiner. 2005. Oral tolerance. Immunol. Rev. 206: 232259.
22. Fazilleau, N.,, L. Mark,, L. J. McHeyzer-Williams, and, M. G. McHeyzer-Williams. 2009. Follicular helper T cells: lineage and location. Immunity 30: 324335.
23. Fotopoulos, G.,, A. Harari,, P. Michetti,, D. Trono,, G. Pantaleo, and, J. P. Kraehenbuhl. 2002. Transepithelial transport of HIV-1 by M cells is receptor mediated. Proc. Natl. Acad. Sci. USA 99: 94109414.
24. Frey, A.,, K. T. Giannasca,, R. Weltzin,, P. J. Giannasca,, H. Reggio,, W. I. Lencer, and, M. R. Neutra. 1996. Role of the glycocalyx in regulating access of microparticles to apical plasma membranes of intestinal epithelial cells—implications for microbial attachment and oral vaccine targeting. J. Exp. Med. 184: 10451059.
25. Haase, A. T. 2005. Perils at mucosal front lines for HIV and SIV and their hosts. Nat. Rev. Immunol. 5: 783792.
26. Handley, S. A.,, R. D. Newberry, and, V. L. Miller. 2005. Yersinia enterocolitxca invasin-dependent and invasin-independent mechanisms of systemic dissemination. Infect. Immun. 73: 84538455.
27. Hase, K.,, T. Murakami,, H. Takatsu,, T. Shimaoka,, M. Iimura,, K. Hamura,, K. Kawano,, S. Ohshima,, R. Chihara,, K. Itoh,, S. Yonehara, and, H. Ohno. 2006. The membrane bound chemokine CXCL16 expressed on follicle-associated epithelium and M cells mediates lympho-epithelial interaction in GALT. J. Immunol. 176: 4351.
28. Helander, A.,, K. J. Silvey,, N. J. Mantis,, A. B. Hutchings,, K. Chandran,, W. T. Lucas,, M. L. Nibert, and, M. R. Neutra. 2003. The viral sigma1 protein and glycoconjugates containing alpha2-3-linked sialic acid are involved in type 1 reovirus adherence to M cell apical surfaces. J. Virol. 77: 79647977.
29. Holmgren, J., and, C. Czerkinsky. 2005. Mucosal immunity and vaccines. Nat. Med. 11: S45S53.
30. Honda, K., and, K. Takeda. 2009. Regulatory mechanisms of immune responses to intestinal bacteria. Mucosal Immunology 2: 187196.
31. Ishikawa, H.,, T. Naito,, T. Iwanaga,, H. Takahashi-Iwanaga,, M. Suematsu,, T. Hibi, and, M. Nanno. 2007. Curriculum vitae of intestinal intraepithelial T cells: their developmental and behavioral characteristics. Immunol. Rev. 215: 154165.
32. Kadaoui, K. A., and, B. Corthesy. 2007. Secretory IgA mediates bacterial translocation to dendritic cells in mouse Peyer’s patches with restriction to mucosal compartment. J. Immunol. 179: 77517757.
33. Kaetzel, C. S. 2005. The polymeric immunoglobulin receptor: bridging innate and adaptive immune responses at mucosal surfaces. Immunol. Rev. 206: 8399.
34. Kagnoff, M. F. 2006. Microbial-epithelial cell crosstalk during inflammation: the host response. Ann. N. Y. Acad. Sci. 1072: 313320.
35. Kelsall, B. 2008. Recent progress in understanding the phenotype and function of intestinal dendritic cells and macrophages. Mucosal Immunology 1: 460469.
36. Kernéis, S.,, A. Bogdanova,, J. P. Kraehenbuhl, and, E. Pringault. 1997. Conversion by Peyer’s patch lymphocytes of human enterocytes into M cells that transport bacteria. Science 277: 948952.
37. Kraehenbuhl, J. P., and, M. R. Neutra. 2000. Epithelial M cells: differentiation and function. Annu. Rev. Cell Dev. Biol. 16: 301332.
38. Kunisawa, J.,, I. Takahashi, and, H. Kiyono. 2007. Intraepithelial lymphocytes: their shared and divergent immunological behaviors in the small and large intestine. Immunol. Rev. 215: 136153.
39. Kunkel, E. J., and, E. C. Butcher. 2003. Plasma-cell homing. Nat. Rev. Immunol. 3: 822829.
40. Lefrançois L., and L. Puddington. 2006. Intestinal and pulmonary mucosal T cells: local heroes fight to maintain the status quo. Annu. Rev. Immunol. 24: 681704.
41. Lo, D.,, W. Tynan,, J. Dickerson,, M. Scharf,, J. Cooper,, D. Byrne,, D. Brayden,, L. Higgins,, C. Evans, and, D. J. O’Mahony. 2004. Cell culture modeling of specialized tissue: identification of genes expressed specifically by follicle-associated epithelium of Peyer’s patch by expression profiling of Caco-2/Raji co-cultures. Internat. Immunol. 16: 9199.
42. Louten, J.,, K. Boniface, and, R. de Waal Malefyt. 2009. Development and function of TH17 cells in health and disease. J. Allergy Clin. Immunol. 123: 10041011.
43. MacPherson, A. J., and, T. Uhr. 2004. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 303: 16621665.
44. MacPherson, A. J.,, K. D. McKoy,, F. E. Johansen, and, P. Brandtzaeg. 2008. The immune geography of IgA induction and function. Mucosal Immunol. 1: 1122.
45. MacPherson, A. J., and, N. L. Harris. 2004. Interactions between commensal intestinal bacteria and the immune system. Nat. Rev. Immunol. 4: 478485.
46. Mantis, N. J., A. Frey, and, M. R. Neutra. 2000. Accessibility of glycolipid and oligosaccharide epitopes on apical surfaces of rabbit villus and follicle-associated epithelium. Am. J. Physiol. (Gastrointest. Liver Physiol.) 278: G915G923.
47. Mantis, N. J.,, M. C. Cheung,, K. R. Chintalacharuvu,, J. Rey,, B. Corthesy, and, M. R. Neutra. 2002. Selective adherence of IgA to murine Peyer’s patch M cells: evidence for a novel IgA receptor. J. Immunol. 169: 18441851.
48. McGhee, J. R.,, M. E. Lamm, and, W. Strober. 2005. Inductive and effector tissues and cells of the mucosal immune system, p. 371–375. In J. Mestecky,, J. Bienenstock,, M. Lamm,, L. Mayer,, J. McGhee, and, W. Strober (ed.), Mucosal Immunology, 3rd ed. Academic Press, San Diego, CA.
49. Mora, J. R.,, M. Iwata,, B. Eksteen,, S. Y. Song,, T. Junt,, B. Senman,, K. L. Otipoby,, A. Yokota,, H. Takeuchi,, P. Ricciardi-Castagnoli,, K. Rajewsky,, D. H. Adams, and, U. H. von Andrian. 2006. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science 314: 11571160.
50. Neutra, M. R.,, and J. P. Kraehenbuhl. 2005. Cellular and molecular basis for antigen transport across epithelial barriers, p. 111–113 In J. Mestecky,, J. Bienenstock,, M. Lamm,, L. Mayer,, J. McGhee, and, W. Strober (ed.), Mucosal Immunology, 3rd ed. Academic Press, San Diego, CA.
51. Neutra, M. R., N. J. Mantis, and, J. P. Kraehenbuhl. 2001. Collaboration of epithelial cells with organized mucosal lymphoid tissues. Nat. Immunol. 2: 10041009.
52. Neutra, M. R., and, P. A. Kozlowski. 2006. Mucosal vaccines: the promise and the challenge. Nat. Rev. Immunol. 6: 148158.
53. Neutra, M. R.,, P. Sansonetti, and, J. P. Kraehenbuhl. 2002. M cells and microbial pathogens, p. 141–156. In M. J. Blaser,, P. D. Smith,, J. I. Ravdin,, H. B. Greenberg, and, L. Guerrant (ed.), Infections of the Gastrointestinal Tract. Raven Press, New York.
54. Niess, J. H., and, H.-C. Reinecker. 2006. Dendritic cells in the recognition of intestinal microbiota. Cell. Microbiol. 8: 558564.
55. Nieuwenhuis, E. E.,, T. Matsumoto,, D. Lindenbergh,, R. Willemsen,, A. Kaser,, Y. Simons-Oosterhuis,, S. Brugman,, K. Yamaguchi,, H. Ishikawa,, Y. Aiba,, Y. Koga,, J. N. Samsom,, K. Oshima,, M. Kikuchi,, J. C. Escher,, M. Hattori,, A. B. Onderdonk, and, R. S. Blumberg. 2009. Cd1d-dependent regulation of bacterial colonization in the intestine of mice. J. Clin. Invest. 119: 12411250.
56. Ouellette, A. J. 2006. Paneth cell alpha-defensin synthesis and function. Curr. Top. Microbiol. Immunol. 306: 125.
57. Pédron, T., and, P. Sansonetti. 2008. Commensals, bacterial pathogens and intestinal inflammation: an intriguing ménage à trois. Cell Host Microbe 3: 344347.
58. Peng, S. L. 2005. Signaling in B cells via Toll-like receptors. Curr. Opin. Immunol. 17: 230236.
59. Peterson, D. A.,, N. P. McNulty,, J. L. Guruge, and, J. I. Gordon. 2007. IgA response to symbiotic bacteria as a mediator of gut homeostasis. Cell Host Microbe 2: 328339.
60. Phalipon, A., and, B. Corthesy. 2003. Novel functions of the polymeric Ig receptor: well beyond transport of immunoglobulins. Trends Immunol. 24: 5558.
61. Qimron, U.,, L. Paul,, E. Bar-Haim, N. Bloushtain,, L. Eisenbach,, H. F. Staats, and, A. Porgador. 2004. Non-replicating mucosal and systemic vaccines: quantitative and qualitative differences in the Ag-specific CD8+ T cell population in different tissues. Vaccine 22: 13901394.
62. Rakoff-Nahoum, S., and, R. Medzhitov. 2008. Innate immune recognition of the indigenous microbial flora. Mucosal Immunol. 1: S10S14.
63. Reinhardt, R. L.,, H. E. Liang, and, R. M. Locksley. 2009. Cytokine-secreting follicular T cells shape the antibody repertoire. Nat. Immunol. 10: 385393.
64. Rescigno, M.,, M. Urbano,, B. Valzasina,, M. Francolini,, G. Rotta,, R. Bonasio,, F. Granucci,, J. P. Kraehenbuhl, and, P. Ricciardi-Castagnoli. 2001. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. 2: 361367.
65. Rimoldi, M.,, M. Chieppa,, V. Salucci,, F. Avogadri,, A. Sonzogni, A,, G. M. Sampietro,, A. Nespoli,, G. Viale,, P. Allavena, and, M. Rescigno. 2005. Intestinal immune homeostasis is regulated by the crosstalk between epithelial cells and dendritic cells. Nat. Immunol. 6: 507514.
66. Russell, M. W.,, and M. Kilian. 2005. Biological activities of IgA, p. 267–290. In J. Mestecky,, J. Bienenstock,, M. Lamm,, L. Mayer,, J. McGhee, and, W. Strober (ed.), Mucosal Immunology, 3rd ed. Academic Press, San Diego, CA.
67. Sakaguchi, S., and, F. Powrie. 2007. Emerging challenges in regulatory T cell function and biology. Science 317: 627629.
68. Sansonetti, P. J. 2006. Rupture, invasion and inflammatory destruction of the intestinal barrier by Shigella: the yin and yang of innate immunity. Can. J. Infect. Dis. Med. Microbiol. 17: 117119.
69. Schneider, P. 2005. The role of APRIL and BAFF in lymphocyte activation. Curr. Opin. Immunol. 17: 282289.
70. Shang L., M. Fukata,, N. Thirunarayanan,, A. P. Martin,, P. Arnaboldi,, D. Maussang,, C. Berin,, J. C. Unkeless,, L. Mayer,, M. T. Abreu, and, S. A. Lira. 2008. Toll-like receptor signaling in small intestinal epithelium promotes B-cell recruitment and IgA production in lamina propria. Gastroenterology 135: 529538.
71. Shastri, N.,, S. Cardinaud,, S. R. Schwab,, T. Serwold, and, J. Kunisawa. 2005. All the peptides that fit: the beginning, the middle, and the end of the MHC class I antigen-processing pathway. Immunol. Rev. 207: 3141.
72. Sierro, F.,, B. Dubois,, A. Coste,, D. Kaiserlian,, J. P. Kraehenbuhl, and, J. C. Sirard. 2001. Flagellin stimulation of intestinal epithelial cells triggers CCL20-mediated migration of dendritic cells. Proc. Natl. Acad. Sci. USA. 98: 1372213727.
73. Sigmundsdottir, H., and, E. C. Butcher. 2008. Environmental cues, dendritic cells and the programming of tissue-selective lymphocyte trafficking. Nat. Immunol. 9: 981987.
74. Trombetta, E. S., and, I. Mellman. 2005. Cell biology of antigen processing in vitro and in vivo. Annu. Rev. Immunol. 23: 9751028.
75. Vasquez-Torres, A.,, J. Jones-Carson,, A. J. Baumler,, S. Falkow,, R. Valdivia,, W. Brown,, M. Le,, R. Berggren,, W. T. Parks, and, F. Fang. 1999. Extraintestinal dissemination of Salmonella by CD18-expressing phagocytes. Nature 401: 804808.
76. Veazey, R. S.,, P. A. Marx, and, A. A. Lackner. 2001. The mucosal immune system: primary target for HIV infection and AIDS. Trends Immunol. 22: 626633.
77. Vijay-Kumar, M., and, A. T. Gewirtz. 2008. Guardians of the gut: newly appreciated role of epithelial toll-like receptors in protecting the intestine. Gastroenterology 135: 351354.
78. Wang, C.,, J. S. McDonough,, K. G. McDonald,, C. Huang, and, R. D. Newberry. 2008. Alpha4beta7/MAdCAM-1 interactions play an essential role in transitioning cryptopatches into isolated lymphoid follicles and a nonessential role in cryptopatch formation. J. Immunol. 181: 40524061.
79. Woof, J. M., and, J. Mestecky. 2005. Mucosal immunoglobulins. Immunol. Rev. 206: 6482.
80. Worbs, T.,, U. Bode,, S. Yan,, M. W. Hoffmann,, G. Hintzen,, G. Bernhardt,, R. Förster, and, O. Pabst. 2006. Oral tolerance originates in the intestinal immune system and relies on antigen carriage by dendritic cells. J. Exp. Med. 203: 519527.
81. Yoshida, M.,, A. Masuda,, T. T. Kuo,, K. Kobayashi,, S. M. Claypool,, T. Takagawa,, H. Kutsumi,, T. Azuma,, W. I. Lencer, and, R. S. Blumberg. 2006. IgG transport across mucosal barriers by neonatal Fc receptor for IgG and mucosal immunity. Springer Semin. Immunopathol. 28: 397403.
82. Zhou, L.,, M. M. Chong, and, D. R. Littman. 2009. Plasticity of CD4+ T cell lineage differentiation. Immunity 30: 646655.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error