
In 2009, a Maryland woman in perfect health discovered a solid, matted lymph node under her left arm. It was biopsied and found to be a malignant melanoma. It had evidently metastasized from a primary tumor somewhere else in her body (melanomas grow from skin cells, and they don't grow directly in lymph nodes). When she underwent scans to appropriately stage her disease, metastatic masses were found everywhere: in lungs, liver, and abdomen. Yet surprisingly, the primary cancer — the origin of her diffuse disease — was never found.
Cases such as hers are relatively rare in oncology. They are called "carcinomas of unknown primary" or CUP. And they usually present a particular thorny therapeutic problem. A major emerging theme in cancer medicine is that every tumor-type is treated differently. Breast, prostate, lung, and uterine cancer are attacked with vastly different regimens of chemicals, and they respond very differently. So how on earth do you treat a cancer of unknown primary?
In this particular case, the woman's tumor cells bore a distinct biological mark indicating their origin in the skin, thereby classifying this as a melanoma. But although that identification brought clarity about the origin of the cancer, it still provided little solace. Metastatic melanoma is one of the few variants of cancer for which no drug or therapy has ever been found to extend survival. Many other forms of cancer have marched ahead in therapeutic terms, notably breast and prostate cancer, lymphomas, and leukemias. Metastatic melanoma, in contrast, seems like a cancer frozen in time. It is likely that the survival of a woman diagnosed in 1609 is no different from a woman diagnosed in 2009.
For decades, oncologists treating metastatic melanoma had a hazy clue about a kind of drug that might work. For reasons mysterious and unknown, some men and women with this cancer experience spontaneous remissions of their melanomas. Their tumors, having grown aggressively, suddenly begin to shrink on their own. The most prominent theory behind these spontaneous remissions was that the immune system was attacking the cancer. And yet, attempts to activate the immune system using drugs had never succeeded in large scale clinical trials.
To understand the mechanism of an immunological attack on cancer, one needs to understand how the immune system works. Immune cells are designed to identify and eliminate foreign elements from the body. They do so by identifying particular markers — called "antigens" — on the foreign cells and attacking these markers. But cancer, of course, grows out of one's own body. It is not "foreign," but a corrupted version of a normal cell. How, then, might the immune system recognize and eliminate a cancerous variant of a normal cell?
Generations of cancer immunologists have tried to answer this question by trying to identify "antigens" that are unique to cancer cells. For some cancers that happen to be caused by viruses, viral antigens might be attacked by the immune system. For other cancers, the answer is more complex. Certain "antigens" in the human body are manufactured only during fetal development, or only in the sperm or testes. For reasons not fully understood, the immune system in adults can recognize these as "foreign." And cancer cells, for yet unknown reasons, begin to manufacture some of these fetal "antigens."
But even so, the immune system does not recognize the fetal antigen on a cancer cell as foreign. To a cancer immunologist, this represents a paradox. Many cancers possess neo-antigens that should be recognized as foreign and thus rejected from the body. And yet, the immune systems seem to be somehow paralyzed in cancer patients so that they fail to reject these cells. In other words, the problem is not the "visibility" of a cancer cell, but rather the blindness of the immune system.
In the 1990s, an immunologist named James Allison hypothesized that the immune system, like many bodily systems, also possesses molecular checks and balances — accelerators and brakes — to prevent inappropriate activation. We know the dire consequences of inappropriate activation: diseases such as rheumatoid arthritis, or multiple sclerosis, in which the immune system begins to attack one's own body. To prevent such gratuitous attacks, the immune system has evolved a sophisticated system of molecular brakes. Many different, independent molecular gates need to be opened in an immunological cell before that cell can be fully activated. The presence of multiple gates acts like a safety latch system, preventing early or inappropriate activation.
Allison was particularly interested in one such gate, a molecule called CTLA4. In the 1990s, Allison and others had shown that blockading CTLA4 in animals could unleash the immune system, allowing these animals to begin rejecting tumors that had been growing in their bodies. In 2008, Allison and others thus launched an enormous study to determine if blockading CTLA4 might work in human cancers. Their obvious choice was melanoma — the tumor in which those tantalizing spontaneous remissions had been observed.
The results, published in the New England Journal of Medicine, tell a tantalizing story. In a randomized double-blinded study, CTLA4 blockade indeed increases the survival of patients with metastatic melanoma. And more: as Allison reminded me last week, this is the only drug that has ever shown an increase in survival in this disease.
The noteworthy feature of this result is that, in principle, any cancer can be treated by the activation of the immune system. Leukemias, lymphomas, breast cancer — anything that might elicit an immune response might be attacked by re-awakened immune cells. Cancer immunologists often refer the immune system as a "sleeping giant." In melanoma, at least, the giant is stirring awake.