Acne: Inflammation. MARK D. FARRAR, PhD EILEEN INGHAM, PhD. P. acnes and Acne. Development of Inflammatory Lesions: Comedogenesis
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1 Acne: Inflammation MARK D. FARRAR, PhD EILEEN INGHAM, PhD Abstract: The inflammatory stage of acne vulgaris is usually of greatest concern to the patient. A number of morphologically different inflammatory lesions may form that can be painful and unsightly. In 30% of patients, such lesions lead to scarring. 1 Inflammatory acne and acne scarring can have significant psychological effects on the patient, including depression, anxiety, and poor self-image. 2 Although inflammatory acne has been well characterized clinically, the mechanisms by which inflammatory lesions arise are still poorly understood. The human skin commensal bacterium, Propionibacterium acnes, has long been associated with inflammatory acne. This organism has been implicated over and above all of the other cutaneous microflora in contributing to the inflammatory response characteristic of acne. However, its precise role in the disease and its interaction with the human immune system remain to be elucidated. P. acnes and Acne P. acnes has been implicated in the pathogenesis of acne for more than 100 years. It was initially believed to be the direct cause of the disease when it was first isolated in 1896, and subsequent studies demonstrating an inflammatory response after injection of P. acnes into the skin reinforced this view. 3,4 However, these findings were cast into doubt when the organism was shown to reside on normal human skin 50 years later. 5 The association between P. acnes and acne has been reaffirmed over the past 30 years through the use of antibiotics for acne treatment. Initial studies showed that antibiotic treatment of acne was therapeutic and resulted in a decrease in the population density of P. acnes on the skin. 6 However, antibiotics are known to be able to modulate the human immune system and thus may have a more direct anti-inflammatory activity. 7 The strongest evidence to date for an association between P. acnes and inflammatory acne came from a study that found erythromycin treatment of acne patients to be therapeutic and that failure of this therapy in a number of individuals was associated with the development of erythromycin resistance in P. acnes. 8 It is now believed that P. acnes is not the cause of acne, but is a significant contributing factor to the inflammatory stages of the disease. Development of Inflammatory Lesions: Comedogenesis Inflammatory lesions develop from comedones arising due to an abnormal pattern of keratinization in the sebaceous follicle. 1 Comedogenesis was once thought to From the Skin Research Centre, Division of Microbiology, School of Biochemistry and Molecular Biology, University of Leeds, Leeds, UK. Address correspondence to Eileen Ingham, PhD, Division of Microbiology, School of Biochemistry and Molecular Biology, University of Leeds, Leeds LS2 9JT, UK. address: E.Ingham@leeds.ac.uk not be part of the inflammatory process, but detailed immunohistological studies that have followed the development of inflammatory acne lesions have shown this to be the first step toward formation of an inflammatory lesion. The microcomedone is now believed to be the earliest type of subclinical acne lesion. Microcomedones develop into full comedones, which may be either open ( blackhead ) or closed ( whitehead ), and inflammatory lesions. Several different types of inflammatory lesion may arise that can be distinguished clinically. Papules and pustules may be up to 5 mm in size with a raised area of erythema. Nodules and cysts are larger lesions that are associated with more severe acne. Nodules may have an inflammatory area of 5 mm or more and persist for several weeks. Cysts may be as large as a few centimeters in size; it is these lesions that often lead to scarring. The resolving stage of an acne lesion is the macule, which is seen clinically as an area of erythema. 9 During comedogenesis, two changes in the normal pattern of keratinization occur: (1) hyperproliferation of keratinocytes lining the follicle wall, as shown by an increase in the cell proliferation marker Ki-67, and (2) reduced desquamation due to increased cohesion between keratinocytes These changes lead to an accumulation of cornified keratinocytes within the follicle. It has been proposed that comedogenesis is a result of changes in the rate of secretion and composition of sebum, most notably a decrease in the concentration of linoleic acid. 13,14 This process may involve cytokines. High levels of biologically active interleukin (IL)-1 have been demonstrated in comedones. 15 This proinflammatory cytokine has been shown to induce hyperkeratinization in isolated sections of the human sebaceous follicle wall (infrainfundibulum) in vitro. 16 The role of P. acnes in comedogenesis is uncertain. Formalin-killed P. acnes cells do not induce normal human keratinocytes to produce IL-1 in vitro. 17,18 However, a more recent study in our laboratory has 2004 by Elsevier Inc. All rights reserved X/04/$ see front matter 360 Park Avenue South, New York, NY doi: /j.clindermatol
2 Clinics in Dermatology Y 2004;22: ACNE: INFLAMMATION 381 demonstrated that viable P. acnes is able to induce human keratinocytes to produce IL-1, tumor necrosis factor (TNF)-, and granulocyte-macrophage colony stimulating factor (GM-CSF). 19 If this process is mirrored in vivo, then P. acnes within the sebaceous follicle may contribute to the process of comedogenesis through IL-1 induced hyperkeratinization. Interestingly, this study demonstrated variations in the stimulation of keratinocytes by P. acnes in different growth phases, with cells in the stationary phase inducing higher levels of cytokines than those in the exponential phase. This may be significant in vivo, because there may be differences in the microenvironment of different sebaceous follicles resulting in different P. acnes growth phases. This may explain why in acne, only a proportion of follicles are affected at any one time. Inflammation: Sequence of Events Debate over the initial cellular infiltrate in inflammatory acne lesions has continued since the first histological studies were carried out years ago. Results of some of the first studies concluded that the lymphocyte was the initiating inflammatory cell type However, Kligman s 1974 study 10 concluded that there was an initial infiltrate of neutrophils followed by microscopic rupture of the sebaceous follicle wall and subsequent formation of a clinically visible inflamed lesion. This course of events is still described in much of the acne literature as the process by which inflamed lesions arise, mediated by neutrophil chemoattractants produced by P. acnes that diffuse through the follicle wall. 23,24 It has been suggested that inflammation in acne results from a type IV hypersensitivity reaction to P. acnes or other comedonal components after the release of reactive oxygen radicals and enzymes by neutrophils and rupture of the follicle wall. 16,23 25 Although it is widely believed that neutrophils are the initial cells infiltrating acne lesions and that these cells initiate inflammation, there is little evidence to support this. More recent histological studies have provided compelling evidence that T lymphocytes are involved in the initiation of inflammation. A 1988 study used lesion mapping to accurately determine the age of inflammatory lesions. 26 This study demonstrated that the initial infiltrate of all developing inflammatory lesions examined consisted of mononuclear cells that were predominantly CD4 T cells. Neutrophils were seen later in the course of inflammation, being detected in 33% of lesions of 72 hours duration. These observations were confirmed in a later study that found CD4 T cells present around lesions of less than 6 hours duration with no disruption of the follicle wall. 27 Neutrophils were seen in only a small proportion of inflamed follicles of greater than 24 hours duration. In addition to characterizing the cellular infiltrate, this study also investigated the expression of various cell surface molecules on cells of the infiltrate and surrounding tissue. Vascular expression of intercellular adhesion molecule-1 (ICAM-1), E-selectin, vascular cell adhesion molecule-1, and human leukocyte associated antigen-dr (HLA-Dr) was observed, as was expression of ICAM-1 and HLA-Dr by cells of the infiltrate and expression of ICAM-1 by follicle wall basal keratinocytes. An extension to these observations was made in a more recent study. 28 Biopsy specimens were obtained from normal sebaceous follicles from individuals without acne, noninflamed follicles from acne patients, and inflamed papules of less than 6 hours duration. Biopsy sections were stained for inflammatory cells, vascular and proliferative markers, integrins, and the proinflammatory cytokine IL-1. Large numbers of CD4 T cells (most of which were memory/effector cells) and macrophages, were seen around uninvolved follicles from acne patients, whereas none were found in non-acne controls. In addition, there was a lack of neutrophils and a reduction in the number of Langerhans cells in the perifollicular epidermis compared with controls. These features are characteristic of a specific immune response. Interestingly, there was an absence of keratinocyte hyperproliferation, and follicles did not display any of the features of microcomedones, suggesting that these inflammatory events are not simply secondary to hypercornification, but may be the earliest events in acne lesion formation. The results of these studies all point toward inflammation being initiated by CD4 T cells and not neutrophils. This would of course suggest that the initiation of inflammation in acne is in response to a specific antigen, as opposed to a nonspecific innate response to comedonal components. Later events in the development of inflammatory lesions include the infiltration of neutrophils and possibly the disruption of the follicle wall. Finally, the inflammatory response is down-regulated, allowing repair of the follicle through normal wound-healing mechanisms. In about 1/3 of individuals, healing of inflamed lesions leads to scarring. 1 The mechanisms behind this process remain unclear, however. The sequence of events in the formation of inflammatory acne lesions is summarized in Figure 1. The Role of P. acnes in Inflammation P. acnes has been shown to be associated with inflammatory acne through antibiotic resistance studies. 6,8 However, this bacterium has not been shown to be a direct cause of the disease or to be involved in the initiation of inflammation. Numbers of viable bacteria within follicles show no correlation with severity of inflammation, and some inflamed lesions do not contain viable P. acnes. 29 However, nonviable P. acnes cells
3 382 FARRAR AND INGHAM Clinics in Dermatology Y 2004;22: Figure 1. Events in the evolution of an inflammatory acne lesion. The normal sebaceous follicle develops into a microcomedone and a comedone through keratinocyte hyperproliferation and reduced sloughing. This process is associated with an increase in levels of IL-1. P. acnes population density increases. Initiation of inflammation may occur through either a specific CD4 T-cell mediated pathway or a nonspecific pathway involving increased production of proinflammatory cytokines by keratinocytes. Inflammation is augmented by activation of macrophages and neutrophils. Finally, the inflammatory response is down-regulated, allowing the lesion to heal. are immunostimulatory. 30 P. acnes produces a number of enzymes and biologically active molecules, some of which have chemoattractant activity, and it has also been shown to stimulate cells of the nonspecific immune system to produce proinflammatory cytokines, for example, the induction of TNF-, IL-1, and IL-8 production by monocytes. 31,32 Recently, P. acnes has been shown to have T-cell mitogenic activity. 33 Such activity could contribute to inflammation in acne through the activation of T cells and the release of immunological cytokines. It has been suggested that toll-like receptors (TLRs) may contribute to inflammation in acne through the activation of TLR2 on macrophages by P. acnes. 34 Activation of TLR on monocytes leads to the release of proinflammatory cytokines IL-12 and IL-8, the latter of which is a neutrophil chemoattractant. TLR2 and TLR4 are expressed on human keratinocytes, and activation leads to IL-8 production. 35,36 A recent review of innate immunity in acne discussed various mechanisms of innate immunity and the role of these mechanisms in inflammation. 37 It has been suggested that P. acnes may contribute to inflammation in acne through activation of TLRs expressed on keratinocytes and sebocytes, which in turn would lead to release of proinflammatory cytokines. In intact follicles, P. acnes will not be in contact with T cells or macrophages; therefore, the aforementioned processes involving activation of these cells by P. acnes are likely to be significant only if rupture of the follicle occurs. Therefore, the direct effects of P. acnes on T cells and macrophages is likely to augment the established immune response rather than initiate it. However, direct contact between P. acnes and viable keratinocytes could occur deep within the follicle where the layer of cornified cells is extremely thin (only two or three cells thick) and extremely fragile. 10 It is here that the interaction between P. acnes and keratinocytes leading to the release of proinflammatory cytokines is more likely to occur. Although it has been shown that P. acnes can activate different arms of the innate immune system, this does not explain why at any one time only a proportion of sebaceous follicles are inflamed and P. acnes can be isolated from unaffected skin and follicles. More important, it does not provide an explanation for the resolution of inflammatory acne. Spontaneous resolution of the disease occurs in most cases when individuals reach their late teens or early twenties. This resolution is not accompanied by a reduction in either the population density of P. acnes on the skin or in the sebum excretion rate, both of which increase at puberty, when the onset of acne is most common. 1,23 Hypotheses and Perspectives The spontaneous resolution of acne is one of the most intriguing features of the disease, and any hypothesis concerning the pathogenesis of acne must attempt to provide an explanation for this event. There is now strong evidence that inflammation in acne is initiated by a specific CD4 T-cell response. The lymphocytic infiltrate observed in early inflammatory lesions could be due to specific recruitment of T cells. Changes in the follicle microenvironment may lead to an increase in the population density of P. acnes within the follicle, with increased production of immunogenic proteins. Such antigens would be processed by Langerhans cells present in the follicle wall. These cells would also be stimulated by the cytokines produced by keratinocytes in response to P. acnes, namely TNF- and GM-CSF. The stimulated Langerhans cells would migrate via the afferent lymph vessels to the local lymph node, where antigens would be presented to CD4 T cells. Subse-
4 Clinics in Dermatology Y 2004;22: ACNE: INFLAMMATION 383 quent activation of these T cells would cause them to migrate to the skin via the efferent lymphatic vessels. At the sebaceous follicle, release of cytokines by these T cells and activation of mononuclear cells would lead to disruption of the follicle and visible inflammation. Clearance of the antigenic stimulus would allow the inflammatory response to be down-regulated and enable the lesion to heal. Conversely, the initial events may be nonspecific and followed by an antigenic-specific response, as was proposed by Holland et al. 38 In this scenario, the increase in sebum production at puberty in certain follicles would lead to a deficiency of linoleic acid within the follicle. An increase in water activity within the follicle due to perturbed barrier function would promote the growth of P. acnes, and the population density would increase. It has been shown that P. acnes can induce IL-1 production by keratinocytes. This may occur deep within the follicle, where the keratinized layers of cells are thinnest and P. acnes may come into contact with viable keratinocytes. In addition, disruption of keratinocytes by extracellular products of P. acnes could also lead to release of IL-1. Diffusion of IL-1 into the surrounding dermis would cause the nonspecific activation of mononuclear and endothelial cells, leading to inflammation and disruption of the follicle. Release of P. acnes antigens into the dermis may then further exacerbate inflammation through activation of CD4 T cells, as described earlier. This cycle of inflammation and resolution of individual follicles may explain the clinical appearance and healing of acne lesions, but it does not explain the complete resolution of the disease. An explanation for this phenomenon may lie with the role of P. acnes in inflammatory acne. The immune response to P. acnes of normal individuals and those suffering from acne has been well characterized. Sensitization to P. acnes has been demonstrated in normal individuals of all ages as well as in acne patients. 1 It has been shown that antibody responses to P. acnes differ between normal individuals and acne patients. Two-dimensional polyacrylamide gel electrophoresis studies have shown that antibodies from acne patients react to a wider range of P. acnes protein antigens than those from normal controls. 39 It should be noted, however, that this increased response to P. acnes may be due to increased exposure to the bacterium as a consequence of the disease. Our current hypothesis on the role of P. acnes in acne is focused on heat-shock proteins (HSPs), which are highly immunogenic. The increase in population density of P. acnes at puberty may put the organisms under nutritional stress in a proportion of follicles. In response to this stress, the organisms may increase production of HSPs, which then activate CD4 T cells via presentation on Langerhans cells. Over time, this response may become negatively regulated due to the high degree of homology between bacterial and human HSPs and the potential for autoreactivity. This hypothesis allows for the initiation of inflammation by either an antigenspecific mechanism or a non antigen-specific mechanism and also offers an explanation for the resolution of acne. To facilitate studies in this area, the genes encoding the two main HSPs of P. acnes, HSP60 (GroEL) and HSP70 (DnaK), have been cloned and sequenced, and the recombinant proteins have been produced in Escherichia coli and purified. 40 Initial immunologic studies have demonstrated the ability of these proteins to induce proinflammatory cytokine production by human keratinocytes in vitro. 19 Future studies should focus on determining whether these proteins play a role in inflammatory acne. Inflammatory acne and its link to P. acnes remains a much underresearched area of cutaneous biology. The precise role of P. acnes in acne and the inflammatory mechanisms involved have yet to be fully elucidated. Further studies into the interaction between the human immune system and P. acnes will hopefully lead to a greater understanding of the pathogenesis of acne and in turn lead to the development of improved treatments for this common disease. There is also a need for more extensive investigations into the more general role of the skin in immunity. How the skin s immune system is modulated by and interacts with commensal skin bacteria is a crucial question in understanding the immune mechanisms that operate in this extremely important arm of the human immune system. References 1. Cunliffe WJ. The sebaceous gland and acne 40 years on. Dermatology 1998;196: Koo JY, Smith LL. Psychologic aspects of acne. Pediatr Dermatol 1991;8: Unna PG. Histopathology of the diseases of the skin. Edinburgh, UK: WF Clay, Acne: Gilchrist TC. The etiology of acne vulgaris. J Cutan Dis Syphil 1903;21: Evans CA, Smith WM, Johnston EA, et al. Bacterial flora of the normal human skin. J Invest Dermatol 1950;15: Thiboutot DM. Acne: an overview of clinical research findings. Dermatol Clin 1997;15: Eady EA, Holland KT, Cunliffe WJ. The use of antibiotics in acne therapy: oral or topical administration. J Antimicrob Chemother 1982;10: Eady EA, Cove JH, Holland KT, et al. Erythromycinresistant propionibacteria in antibiotic-treated acne patients: association with therapeutic failure. Br J Dermatol 1989;121: Cunliffe WJ. Acne. In: Marks R, editor. Clinical features of acne. London: Martin Dunitz, 1989 Chapter Kligman AM. An overview of acne. J Invest Dermatol 1974;62:
5 384 FARRAR AND INGHAM Clinics in Dermatology Y 2004;22: Plewig G, Fulton JE, Kligman AM. Cellular dynamics of comedo formation in acne vulgaris. Arch Dermatol Forsch 1971;242: Knaggs HE, Holland DB, Morris C, et al. Quantification of cellular proliferation in acne using the monoclonal antibody Ki-67. J Invest Dermatol 1994;102: Downing DT, Stewart ME, Wertz PW, et al. Essential fatty acids in acne. J Am Acad Dermatol 1986;14: Morello AM, Downing DT, Strauss JS. Octadecadienoic acids in the skin surface lipids of acne patients and normal subjects. J Invest Dermatol 1976;66: Ingham E, Eady EA, Goodwin CE, et al. Proinflammatory levels of interleukin-1 like bioactivity are present in the majority of open comedones in acne vulgaris. J Invest Dermatol 1992;98: Guy R, Kealey T. Modelling the infundibulum in acne. Dermatology 1998;196: Walters CE, Ingham E, Eady EA, et al. In vitro modulation of keratinocyte-derived interleukin-1 (IL-1 ) and peripheral blood mononuclear cell-derived IL-1 release in response to cutaneous commensal microorganisms. Infect Immun 1995;63: Ingham E, Walters CE, Eady EA, et al. Inflammation in acne vulgaris: failure of skin microorganisms to modulate keratinocyte interleukin-1 production in vitro. Dermatology 1998;196: Graham GM, Farrar MD, Cruse-Sawyer JE, et al. Proinflammatory cytokine production by human keratinocytes stimulated with Propionibacterium acnes and P. acnes GroEL. Br J Dermatol, 2004;150: Strauss JS, Pochi PE. Intracutaneous injection of sebum and comedones: histological observations. Arch Dermatol 1965;92: Lynch FW. Acne vulgaris: a review of histologic changes observed in early lesions. Arch Dermatol Syphil 1940;42: Vasarinsh P. Keratinization of pilar structures in acne vulgaris and normal skin. Br J Dermatol 1969;81: Leyden JJ, McGinley KJ, Vowels B. Propionibacterium acnes colonization in acne and non-acne. Dermatology 1998;196: Webster GF. Inflammatory acne represents hypersensitivity to Propionibacterium acnes. Dermatology 1998;196: Akamatsu H, Horio T. The possible role of reactive oxygen species generated by neutrophils in mediating acne inflammation. Dermatology 1998;196: Norris JBF, Cunliffe WJ. A histological and immunocytochemical study of early acne lesions. Br J Dermatol 1988; 118: Layton AM, Morris C, Cunliffe WJ, et al. Immunohistochemical investigation of evolving inflammation in lesions of acne vulgaris. Exp Dermatol 1998;7: Jeremy AH, Holland DB, Roberts SG, Thomson KF, Cunliffe WJ. Inflammatory events are involved in acne lesion initiation. J Invest Dermatol 2003;121: Leeming JP, Holland KT, Cunliffe WJ. The microbial colonization of inflamed acne vulgaris lesions. Br J Dermatol 1988;118: Eady EA, Ingham E. Propionibacterium acnes friend or foe? Rev Med Microbiol 1994;5: Chen Q, Koga T, Uchi H, et al. Propionibacterium acnes induced IL-8 production may be mediated by NF- B activation in human monocytes. J Dermatol Sci 2002;29: Vowels BR, Yang S, Leyden JJ. Induction of proinflammatory cytokines by a soluble factor of Propionibacterium acnes: implications for chronic inflammatory acne. Infect Immun 1995;63: Jappe U, Ingham E, Henwood J, et al. Propionibacterium acnes and inflammation in acne: P. acnes has T-cell mitogenic activity. Br J Dermatol 2002;146: Kim J, Ochoa MT, Krutzik SR, et al. Activation of toll-like receptor 2 in acne triggers inflammatory cytokine responses. J Immunol 2002;169: Kawai K, Shimura H, Minagawa M, et al. Expression of functional toll-like receptor 2 on human epidermal keratinocytes. J Dermatol Sci 2002;30: Pivarcsi A, Bodai L, Rethi B, et al. Expression and function of toll-like receptors 2 and 4 in human keratinocytes. Int Immunol 2003;15: Koreck A, Pivarcsi A, Dobozy A, et al. The role of innate immunity in the pathogenesis of acne. Dermatology 2003; 206: Holland KT, Aldana O, Bojar RA, et al. Propionibacterium acnes and acne. Dermatology 1998;196: Holland KT, Holland DB, Cunliffe WJ, et al. Detection of Propionibacterium acnes polypeptides which have stimulated an immune response in acne patients but not in normal individuals. Eur J Exp Dermatol 1993;116: Farrar MD, Ingham E, Holland KT. Heat-shock proteins and inflammatory acne vulgaris: molecular cloning, overexpression and purification of a Propionibacterium acnes GroEL and DnaK homologue. FEMS Microbiol Lett 2000; 191:183 6.
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